THE MACHINERY FOR CELL POLARITY, CELLMORPHOGENESIS, AND THE CYTOSKELETON IN THEBASIDIOMYCETE FUNGUS Ustilago maydis A SURVEY OF THEGENOME SEQUENCE#

Flora Banuett1,*, Rene H. Quintanilla Jr.1,&, and Cristina G. Reynaga-Peña2

1,*Department of Biological Sciences, California State University, 1250 Bellflower Boulevard, Long Beach,CA 90840, Phone: (562)-985-5535. email: fbanuett@csulb.edu

1,&Department of Biological Sciences, California State University, 1250 Bellflower Boulevard, Long Beach,CA 90840, email: rquintan@csulb.edu

2Departamento de Ingeniería Genética, Centro de Investigación y de Estudios Avanzados del IPN, UnidadIrapuato, Campus, Guanajuato, Irapuato, Gto. CP 36821 MEXICO, Phone: +52 (462) 623-9653, e-mail:creynaga@ira.cinvestav.mx

AbstractUstilago maydis, a Basidiomycete fungus that infects maize, exhibits two basic morphologies, ayeast-like and a filamentous form. The yeast-like cell is elongated, divides by budding, and the budgrows by tip extension. The filamentous form divides at the apical cell and grows by tip extension.The repertoire of morphologies is increased during interaction with its host, suggesting that plantsignals play an important role in generation of additional morphologies. We have used S.cerevisiae and S. pombe genes known to play a role in cell polarity and morphogenesis, and in thecytoskeleton as probes to survey the U. maydis genome. We have found that most of the yeastmachinery is conserved in U. maydis, albeit the degree of similarity varies from strong to weak. TheU. maydis genome contains the machinery for recognition and interpretation of the budding yeastaxial and bipolar landmarks; however, genes coding for some of the landmark proteins are absent.Genes coding for cell polarity establishment, exocytosis, actin and microtubule organization,microtubule plus-end associated proteins, kinesins, and myosins are also present. Genes not presentin Saccharomyces cerevisiae and Schizosaccharomyces pombe include a homologue of mammalianRac, a hybrid myosin-chitin synthase, and several kinesins that exhibit more similarity to theirmammalian counterparts. We also used the U. maydis genes identified in this analysis to search otherfungal and other eukaryotic genomes to identify the closest homologues. In most cases, notsurprisingly, the closest homologue is among filamentous fungi, not the yeasts, and in some cases itis among mammals.

Correspondence to: Flora Banuett.#In memoriam Ira HerskowitzPublisher's Disclaimer: This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customerswe are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resultingproof before it is published in its final citable form. Please note that during the production process errors may be discovered which couldaffect the content, and all legal disclaimers that apply to the journal pertain.

NIH Public AccessAuthor ManuscriptFungal Genet Biol. Author manuscript; available in PMC 2009 August 1.

Published in final edited form as:Fungal Genet Biol. 2008 August ; 45(Suppl 1): S3–S14. doi:10.1016/j.fgb.2008.05.012.

NIH

-PA Author Manuscript

NIH

-PA Author Manuscript

NIH

-PA Author Manuscript

Keywordspolarized growth; cytoskeleton; polarisome; fungal morphogenesis

I. OVERVIEW OF CELL POLARITY AND CELL ORPHOGENESISCell polarity is a fundamental biological process by which asymmetry of cell components(cytoskeleton, cell organelles, and membrane domains) is generated. Polarization of cellcomponents occurs in diverse cells in response to endogenous programming and to externalcues. This cellular asymmetry is important in determining cell morphogenesis and the planeof cell division in a variety of eukaryotic cells, and is crucial for development of metazoans.Studies in budding yeast and fission yeast have been instrumental in identification of themachinery involved in cell polarity and morphogenesis. These studies indicate that recognitionof a spatial landmark triggers assembly of protein complexes that initiate assembly andpolarization of the actin cytoskeleton, which directs vesicle delivery to sites of growth.

Fungal filaments (hyphae) exhibit continuous polarized growth at their tips. New axes ofpolarized growth (branches) are established along the main axis of polarized growth. Currentwork in filamentous fungi aims to understand the molecular mechanisms that determine: (a)the axis of polarized growth, (b) new axes of cell polarity, and (c) the site of cytokinesis andseptum formation. The availability of the genome sequences of fungi from across the differentsubdivisions of the kingdom, together with improved tools for generation of knock out strains,regulatable gene expression, and sophisticated imaging techniques promise to reveal newinsights about polarized growth and cell morphogenesis in filamentous fungi, and will likelylead in the future to the generation of protein interaction maps for this machinery as has beendone in Saccharomyces cerevisiae (Drees et al., 2001).

Here we explore the genome sequence of Ustilago maydis in search of homologues of genesknown to play crucial roles in cell morphogenesis and cell polarity in the yeasts. We firstprovide a synopsis of the morphologies that characterize U. maydis growth in culture and inthe plant. We follow with a brief summary of key players of polarized growth in S.cerevisiae, and indicate which components of the machinery are conserved in U. maydis, andwhere known, describe their role in polarized growth. We conclude from our analysis that mostof the yeast machinery is conserved in U. maydis, as it is in other filamentous fungi (Harris,2006; Philippsen et al., 2005), and in many instances it is used in novel ways.

II. OVERVIEW OF THE MORPHOLOGICAL TRANSITIONS IN THE LIFE CYCLEOF U. maydis

Ustilago maydis is a Basidiomycete fungus that infects maize (Zea mays L) and teosinte (Zeamays spp. mexicana or spp. parviglumis). The fungus exhibits two basic morphologies and iscapable of switching from one form to the other (the dimorphic switch) (Fig. 1). This switchis crucial to pathogenicity. The yeast-like form is unicellular, haploid, divides by budding, andis nonpathogenic; the filamentous form is dikaryotic, grows by tip extension, and is pathogenic(reviewed in Banuett, 1995;2002;Christensen, 1963;Holliday, 1974;Klosterman et al., 2007).The dimorphic switch and other aspects of the life cycle are controlled by two unlinked matingtype loci, a and b. The a locus codes for components of a signal transduction pathway(pheromone precursor and receptor genes) and the b locus codes for a combinatorialhomeodomain protein. The a locus governs cell fusion of haploid cells and filamentous growthof the dikaryon in vitro but not in planta; the b locus is the major determinant of filamentousgrowth, in vitro and in planta, and of pathogenicity (reviewed in Banuett, 2002;2007;Klosterman et al., 2007). In order to complete the life cycle, haploids that fuse must differ

Banuett et al. Page 2

Fungal Genet Biol. Author manuscript; available in PMC 2009 August 1.

NIH

-PA Author Manuscript

NIH

-PA Author Manuscript

NIH

-PA Author Manuscript

at both a and b (for example, a1 b1 + a2 b2). The a locus has two alleles (a1 and a2) and theb locus 25 naturally occurring alleles (b1....b25), and any combination of different b allelesresults in an active b protein (reviewed in Banuett 2002;2007;Klosterman et al., 2007).

The repertoire of morphologies is expanded by interaction of U. maydis with its hosts (Fig. 1).This is evidenced by the formation of a specialized structure for penetration, the appressorium,(see for example, Brachmann et al., 2003; Snetselaar and Mims, 1993), by extensive branchingon the leaf surface and inside plant cells (Banuett and Herskowitz, 1996), and by formation ofclamp-like structures for nuclear distribution (Scherer et al., 2006). Appressoria, branchformation, and clamp-like structures are not observed in culture. Once tumors are formed,dikaryotic hyphae undergo a discrete developmental program characterized by distinctmorphologies (cylindrical cells, spherical cells, and other diverse shapes) that arise upon hyphalfragmentation and lead to formation of the teliospore, a round spore with a specialized cellwall (Fig. 1) (Banuett and Herskowitz, 1996). The distinct cell morphologies present in theplant are not observed in vitro. It has thus been proposed that the plant produces signals thattrigger fungal differentiation and reorganization of the machinery for polarized growth(Banuett and Herskowitz, 1996). The nature of these signals is not known. Interestingly, thefungus also elicits changes in cell morphology and nuclear position of the host (Banuett andHerskowitz, 1996;Ruiz-Herrera et al., 1999; reviewed in Banuett, 2002). Thus, the interactionof U. maydis with its host appears to be a reciprocal process of signal exchange that results inalterations in cell morphology of both host and fungus.

A. The yeast-like cell morphologyThe yeast-like cells are elongated with tapered ends (cigar-shaped). They bud once per cellcycle at one of the cell poles. The mechanism by which one of the cell poles is chosen versusthe other is not known. Cells are able to bud at new sites at the cell poles or use a previouslychosen site for budding as in apiculate yeasts (Jacobs et al., 1994). In some respects this patternresembles the bipolar budding pattern of S. cerevisiae. The U. maydis bud grows by tipextension (Banuett and Herskowitz, 2002). There is no phase of isotropic growth, whichcontrasts with bud growth in S. cerevisiae where there is a short phase of polarized growthearly in the cell cycle followed by a switch to isotropic growth in the G2/M phase of the cellcycle (reviewed in Pruyne and Bretscher, 2000a,b). Formation of the U. maydis bud entailsseveral morphological steps that result in the final shape of the bud (Banuett and Herskowitz,2002).

B. The filamentous formIn culture, the filamentous form grows by tip extension, as occurs in other filamentous fungi,and divides at the apical cell to produce an actively growing tip cell and a subapical cell devoidof cytoplasm, but little is known about division of the apical cell. In planta, most hyphalcompartments, not just the tip cell, contain cytoplasm (Banuett and Herskowitz, 1996) andnuclear distribution involves clamp-like structures (Scherer et al., 2006).

C. The Spitzenkörper and filamentous growthFungal hyphae exhibit continuous polarized growth; there is no arrest of growth duringcytokinesis. Examples of cells that exhibit such highly polarized growth are pollen tubes androot hairs in plants, and neurons in animals.

In filamentous fungi, a fungal-specific phase-contrast opaque body, the Spitzenkörper (apicalbody), located at or just below the tip of the apical cell, is thought to drive hyphal growth(López-Franco, 1996; Reynaga-Peña et al., 1997). It consists of a heterogeneous population ofvesicles surrounding a core that contains polysomes, microtubules, and actin, and is proposedto serve as a supply center for the distribution of vesicles containing materials necessary for

Banuett et al. Page 3

Fungal Genet Biol. Author manuscript; available in PMC 2009 August 1.

NIH

-PA Author Manuscript

NIH

-PA Author Manuscript

NIH

-PA Author Manuscript

tip extension (reviewed in Bartnicki-García, 2002; Harris et al., 2005; Harris, 2006). TheSpitzenkörper can be visualized with the amphiphilic styryl dye FM4-64 (Fischer-Parton et al,2000). Long-range transport of vesicles from other parts of the hypha to the Spitzenkörper isproposed to occur along microtubules, and delivery from the Spitzenkörper to sites of growthis proposed to occur on actin tracks (reviewed in Harris et al., 2005; Harris, 2006). Bothmicrotubules and actin are necessary for hyphal morphogenesis. Disruption of microtubules,kinesin, dynein, and dynactin results in unstable axes of polarized growth but not in absenceof polarized growth per se, whereas disruption of actin causes complete loss of cell polarityand results in isotropic growth (Harris et al., 2005; Heath, 2000; Lee et al., 2001; Riquelme etal., 2000; Rupes et al., 1995; Seiler et al., 1999; Torralba et al., 1998a,b; Virag and Griffiths,2004). Some of these conditions also result in loss or alteration of the position or function ofthe Spitzenkörper (Crampin et al., 2005; Konzack et al., 2005; Riquelme et al., 2000; Seiler etal., 1999).

There is a dearth of information concerning the molecular composition of the Spitzenkörper.Recent work in different filamentous fungi indicates that formin (a multidomain, actin-nucleating protein), myosin light chain, Sec4 (a Rab GTPase), BemA (homologue of S.cerevisiae Bem1), TeaA and TeaR (homologues of S. pombe end cell markers Tea1 and Mod5,respectively), and two chitin synthases are components of the Spitzenkörper (see below)(Crampin et al., 2005; Leeder and Turner, 2007; Riquelme et al., 2007; Sharpless and Harris,2000; Takeshita et al., 2008). The presence of formin suggests that the Spitzenkörper may serveas an actin nucleation center. Little is known about the Spitzenkörper in U. maydis.

III. U. maydis HOMOLOGUES OF YEAST GENES INVOLVED IN CELLPOLARITY AND CELL MORPHOGENESIS

The yeasts, S. cerevisiae and Schizosaccharomyces pombe have been used extensively instudies of cell polarity and morphogenesis (Chang and Peter, 2003). These studies provide theframework in which to understand these processes in other organisms, in particular the fungi;therefore, we have used these two yeasts as a reference point in our analysis. Below we describesome of the components of the machinery for polarized growth in S. cerevisiae (for S.pombe see supplementary material), and identify components conserved in U. maydis. Wedescribe, where known, their function in U. maydis, and in some filamentous fungi.

A. A hierarchy of GTPase modules controls bud site selection and establishment of polarizedgrowth in S. cerevisiae

1. Recognition of the spatial landmark—S. cerevisiae cells divide by budding andexhibit two budding patterns, axial and bipolar, which are genetically determined by theMAT locus. a or α cells exhibit the axial budding pattern, in which mother and daughter cellsbud immediately adjacent to the previous budding site. a/α cells exhibit a bipolar buddingpattern, in which daughters bud distally to the site of their birth, whereas the mother can buddistally or proximally to the previous budding site (reviewed in Casamayor and Snyder,2002; Chant, 1999). A GTPase module consisting of a Ras-like GTPase Rsr1/Bud1, its guaninenucleotide exchange factor (GEF) Bud5, and its GTPase-activating protein (GAP) Bud2determine the site of budding in response to a spatial landmark for axial or bipolar budding(reviewed in Casamayor and Snyder, 2002; Chant, 1999). The landmark for axial buddingconsists of septins, Bud3, Bud4, Axl1, Bud10/Axl2, and for bipolar budding of Bud8, Bud9,Bud7, Rax1, and Rax2. The Rsr1/Bud1 GTPase module is not essential for viability; in itsabsence cells are still capable of polarized growth but in a random manner (reviewed inCasamayor and Snyder, 2002; Chant, 1999; Park and Bi, 2007).

Banuett et al. Page 4

Fungal Genet Biol. Author manuscript; available in PMC 2009 August 1.

NIH

-PA Author Manuscript

NIH

-PA Author Manuscript

NIH

-PA Author Manuscript

2. Polarity establishment and the Cdc42 GTPase module—The Rsr1/Bud1 GTPasemodule interprets the spatial landmark (axial or bipolar) and recruits another GTPase modulethat consists of the Rho GTPase Cdc42, its guanine nucleotide exchange factor (GEF) Cdc24,and its GTPase-activating proteins (GAPs) Bem3 and Rga1/2 (reviewed in Casamayor andSnyder, 2002; Chant, 1999; Park and Bi, 2007). This module in turn recruits the actincytoskeleton, which polarizes secretion towards the site of growth (reviewed in Pruyne andBretscher, 2000a,b).

B. U. maydis homologues of landmark proteins and the BUD site selection and polarityestablishment GTPase modules

The U. maydis genome lacks coding information for homologues of Bud3 and Bud4 (axiallandmark), and Bud8 and Bud9 (bipolar landmark) (Table 1), but contains the information forBud10/Axl2 (axial landmark), and Rax1 and Rax2 (bipolar landmark). Thus, U. maydiscontains a subset of the genes that code for the axial and bipolar landmark proteins. Their rolein budding and cell morphogenesis remains to be determined. Interestingly, in Ashbyagossypii, a filamentous fungus closely related to S. cereviasae, AgBud3 appears to act as alandmark for septation (Wendland, 2003). Coding information for components of the Rsr1/Bud1 GTPase module (Rsr1/Bud1, Bud2, and Bud5) and many other recently identified genesrequired for bipolar budding (BUD13-32;Ni and Snyder, 2001) is present in the U. maydisgenome (Table 1). The function of these genes remains to be determined. In A. gossypii,AgRsr1/Bud1 is required for actin organization, for normal hyphal growth and branching, andfor position of the polarisome component AgSpa2. Control of the position of a polarisomecomponent by the Rsr1/Bud1 GTPase is a novel function of this GTPase. The Agrsr1 nullmutant is characterized by false branch initiation, pausing and reinitiation of growth resultingin bulges along the hypha, and transient appearance and disappearance of AgSpa2 thatcorrelates with phases of pausing and growth (Bauer et al., 2004). In wild type hyphae, AgSpa2(a homologue of S. cerevisiae Spa2, see below) is present at the hyphal tip continuously. InCandida albicans, another fungus closely related to S. cerevisiae, CaRsr1/Bud1 defects resultin random budding in yeast cells and in defects in germ tube emergence (Yaar et al., 1997).

The U. maydis genome contains coding information for homologues of the Rho Cdc42 GTPasemodule (Cdc42, Cdc24, Bem3, Rga1/2) (Table 1). In addition, U. maydis, like otherfilamentous fungi, contains a homologue of mammalian Rac, another Rho GTPase, which isabsent from the genomes of S. cerevisiae and S. pombe. In mammals, Cdc42 and Rac1 playpartially overlapping roles in morphogenesis, cell division, and migration (Jaffe and Hall,2005). Likewise in filamentous fungi, Cdc42 and Rac appear to have partially overlappingfunctions in control of cell polarity (see for example, Bassilana and Arkowitz, 2006;Boyce etal., 2001,2003;Chen and Dickman, 2004;2006;Rolke and Tudzynski, 2008;Scheffer et al.,2005;Virag et al., 2007).

In U. maydis, Cdc42 is required for cell separation but not for polarized growth, and is notessential for viability (Mahlert et al., 2006; F. Banuett, unpublished results), whereas UmRac1is required for normal cell morphology of the yeast-like cell and for positioning of the septum(Mahlert et al., 2006). Umcdc42 null mutants form chains of cells that exhibit wild typemorphology, separated by a single septum (Mahlert et al., 2006). In wild type cells, there aretwo septa prior to cell separation, one on the mother side and the other on the bud side. Cellseparation occurs in the region between these two septa, the fragmentation zone (Banuett andHerskowitz, 2002; O’Donnell and McLaughlin, 1984; Weinzierl et al., 2002). In S. cerevisiaeCDC42 is essential for viability and for polarity establishment: cdc42ts and cdc24 mutantsarrest as large unbudded, multinucleate cells (reviewed in Pruyne and Bretscher, 2000a,b).Thus, U. maydis and S. cerevisiae use Cdc42 differently, a theme repeated in other filamentousfungi (see below).

Banuett et al. Page 5

Fungal Genet Biol. Author manuscript; available in PMC 2009 August 1.

NIH

-PA Author Manuscript

NIH

-PA Author Manuscript

NIH

-PA Author Manuscript

The importance of Rac1 in polarized growth is supported by the following observations:expression of an activated allele of Rac1 results in formation of balloon-like structures at thetips of yeast-like cells; and Umrac1 null mutants exhibit elongated abnormal cells with roundedends and a septum in the middle; wild type cells, in contrast, have tapered ends (Mahlert et al.,2006). UmRac1 is not required for cell viability, but depletion of UmRac1 in a strain lackingUmcdc42 is lethal: cells arrest as chains of enlarged, aberrant cells, with a single nucleus, anddelocalized cell wall material (Mahlert et al., 2006). This observation suggests that Cdc42 andRac1 share a common target. Rac1 is also necessary for the b-dependent transition from yeast-like to filamentous form: induction of Umrac1 expression in haploid cells (haploids normallylack an active b protein) causes a transition from yeast-like to filamentous form. UmRac1 isthus necessary and sufficient for the dimorphic switch that results in filament formation(Mahlert et al., 2006). The GEF and GAP regulators of the UmRac1 GTPase remain to beidentified.

In Aspergillus nidulans Cdc42 is required for hyphal morphogenesis, but it is not required forlocalization of polarisome components, the Spitzenkörper, or organization of actin, and neitheris AnRac1 required for localization of polarisome components or the Spitzenkörper (Virag etal., 2007). In contrast, S. cerevisiae Cdc42 is required for localization of polarisomecomponents and actin organization (reviewed in Chang and Peter, 2003; Pruyne and Bretscher,2000a, b). AnCdc42 and AnRac likely share a common target because double Anrac1Ancdc42 mutants are synthetic lethal: the double mutants are unable to polarize and lyse asattached rounded cells separated by septa (Virag et al., 2007). In Penicillium marneffei, Rac isrequired for normal organization of the actin cytoskeleton. Rac regulates polarized growth ofthe hypha in concert with Cdc42 but the specific steps controlled by these Rho GTPases differ(Boyce et al., 2001, 2003). The synthetic lethality of cdc42 and rac1 in U. maydis and otherfilamentous fungi supports the notion that these Rho GTPases play partially overlapping rolesin control of cell polarity.

C. U. maydis homologues of effectors of Cdc42In S. cereviasiae, downstream effectors of Cdc42 include the p21-activated kinases (PAKs)Cla4, Ste20, and Skm1, and two proteins of unknown function, Gic1 and Gic2 (reviewed inPruyne and Bretscher, 2000a, b). Ste20 and Cla4 are important for the Cdc42-dependentreorganization of the actin cytoskeleton during the cell cycle. The U. maydis genome containscoding information for three Ste20-like kinases (Table 1): Smu1, Cla4, and Don1, but not forGic1 and Gic2. Smu1 and Cla4 contain the CRIB domain present in p21-activated kinases(PAKs), whereas Don1 lacks this domain, and thus belongs to the germinal center (GCK)subfamily of Ste20-like kinases (Leveleki et al., 2004; Smith et al., 2004). (For further detailson Smu1, see the article by García-Pedrajas et al. in this issue). Both UmDon1 and UmCla4play a role in cytokinesis (Leveleki et al., 2004), just as Cla4 and Ste20 do in S. cerevisiae.Two observations support the idea that UmCla4 is likely to be a downstream effector ofUmRac1: both Δcla4 and Δrac1 mutants have a similar phenotype, and they show yeast two-hybrid interactions. Other effectors of Rac1 are likely to exist because Δcla4 does not suppressthe lethality observed upon expression of an activated allele of Rac1 (Mahlert et al., 2006).

D. U. maydis homologues of other Rho proteinsThe Rho subfamily of GTPases includes Rho, Rac, Cdc42, and others. They act as molecularswitches that play important roles in cell polarity, morphogenesis, and cell division (Jaffe andHall, 2005). S. cerevisiae contains one Cdc42 (described above) and five Rho proteins, Rho1-5.Rho1, an essential gene for viability, is required for polarity establishment. Rho3 and Rho4are also required for polarized growth. The signal from different Rho proteins (Rho1, Rho3,Rho4, and Cdc42) converges on the formin Bni1, a polarisome component, to control actinorganization (see below) (Dong et al., 2003; reviewed in Pruyne and Bretscher, 2000a,b). In

Banuett et al. Page 6

Fungal Genet Biol. Author manuscript; available in PMC 2009 August 1.

NIH

-PA Author Manuscript

NIH

-PA Author Manuscript

NIH

-PA Author Manuscript

addition, Rho1 controls bud morphogenesis via two different outputs: as a catalytic subunit ofβ-glucan synthase, the enzyme that synthesizes the major component of the cell wall, and asan activator of protein kinase C (Pkc1) that controls the cell wall integrity signal transductionpathway (reviewed in Banuett, 1998; Cabib et al., 1998; Pruyne and Bretscher, 2000a,b). Theregulators of Rho1 include two redundant GEFs, Rom1 and Rom2, and two GAPs, Sac7 andBem3. The U. maydis genome contains coding information for three Rho proteins, Rho1, Rho2,and Rho3, and for homologues of Rho1 regulators (Table 1). Their function has not beenreported. Rho proteins in other filamentous fungi are required for polarized growth and it islikely that this function will be conserved in U. maydis. In A. gossypii, rho3 mutants exhibitswelling of hyphal tips indicative of isotropic growth, and rho1 null mutants exhibit lysis ofcells in a colony (Wendland and Philippsen, 2001). In A. nidulans, RhoA, a homologue of S.cerevisiae Rho1, is necessary for polarized growth, branching pattern, and cell wall deposition(Guest et al., 2004).

E. U. maydis homologues of polarisome componentsIn S. cerevisiae, the polarity determining proteins, Spa2, Pea2, Bud6/Aip3, and Bni1, assembleat the bud tip and function as a scaffold for the assembly of other proteins. Mutants lackingeither of these proteins exhibit defects in actin organization, apical growth, and have widenednecks (reviewed in Pruyne and Bretscher, 2000a,b). The polarisome links Rho GTPases andactin cable assembly through the formin Bni1. Formins are multidomain proteins required formaintenance of cell polarity, cytokinesis, and actin organization, and are central to how inputsfrom Rho GTPases are transmitted to actin organization (Chang and Peter, 2003; Evangelistaet al., 2003; Wallar and Alberts, 2003). Bni1 binds profilin, an actin-monomer binding protein,and has been shown to nucleate actin cables. Bud6 is important for the Bni1 actin-nucleationfunction (Pruyne et al., 2002; Sagot et al., 2001). Localization of Bni1 to the bud tip requiresSpa2 and Pea2. Some polarisome components also localize to the mother-bud neck regionduring cytokinesis to participate in formation of the actomyosin ring and the septum (reviewedin Pruyne and Bretscher, 2000a,b).

The U. maydis genome contains coding information for homologues of polarisome componentsBud6, Spa2, and two formins, UmSepA and UmDia, but not of Pea2 (Table 1). The role ofthese proteins in cell polarity of the yeast-like and filamentous form in U. maydis remains tobe determined. Recent studies in A. gossypii, A. nidulans, and C. albicans (Crampin et al.,2005;Knechtle et al., 2003;Virag and Harris, 2006) are providing insights about the role of thepolarisome complex in polarized growth of the hypha. In A. nidulans, homologues of Spa2,Bud6/Aip3, and Bni1 are necessary for maintaining the axis of polarized growth: mutations ineither component result in dichotomous branching (branching at the hyphal tip), which isnormally not observed in wild type hyphae (Sharpless and Harris, 2002;Virag and Harris,2006). SpaA::GFP localizes to the hyphal tip, overlapping to some extent the localization ofthe Spitzenkörper, consistent with a role at the hyphal tip, possibly as a component of theSpitzenkörper (Virag and Harris, 2006). SpaA is not required for localization of the forminSepA (Virag and Harris, 2006), whereas S. cerevisiae Spa2 is required for localization of theformin Bni1 (reviewed in Pruyne and Bretscher, 2000a,b). BudA, the A. nidulans homologueof Bud6/Aip3, localizes to sites of septum formation. The AnbudA mutant phenotype isconsistent with a role in maintenance of the axis of polarized growth and determining the areaof growth. AnbudA null mutants exhibit reduced hyphal growth rate, increased hyphal diameterand nuclei per hyphal segment, dichotomous branching, and increased branching frequency,and potato-shaped germlings (Virag and Harris, 2006). AnSepA is required for septumformation, for maintenance of the axis of polarized growth, and determining the area of growth,and normal organization of actin at the hyphal tips and septa. SepA null mutants exhibit widerhyphal diameter, dichotomous branching, and lack septa. SepA::GFP localizes to hyphal tips,coincident with localization of the Spitzenkörper, and also to septa (Sharpless and Harris,

Banuett et al. Page 7

Fungal Genet Biol. Author manuscript; available in PMC 2009 August 1.

NIH

-PA Author Manuscript

NIH

-PA Author Manuscript

NIH

-PA Author Manuscript

2002). This localization led to the hypothesis that the Spitzenkörper acts as an actin-nucleatingcenter (Sharpless and Harris, 2002).

In A. gossypii, the Spa2 homologue, which localizes permanently to the hyphal tip and to sitesof branch initiation, appears to determine area of growth, normal growth rate, and branchingdensity (Knechtle et al., 2003). AgBNI1 is necessary for establishment of polarized growth andfor actin organization. Disruption of AgBNI1 results in formation of giant potato-shaped cellslacking actin cables and also in the inability to form hyphae (Schmitz et al., 2006). AgBni1localizes to hyphal tips. A constitutively active AgBni1 results in dichotomous hyphalbranching in young hyphae, a type of branching normally restricted to mature hyphae (Schmitzet al., 2006). The localization of these proteins at the hyphal tip supports a role in determiningpolarized growth.

In C. albicans, CaBni1 and CaMlc1 (myosin light chain) colocalize with the Spitzenkörper,whereas Spa2 and Bud6/Aip3 localize mostly as a cap at the hyphal tip that overlays theSpitzenkörper (Crampin et al., 2005). Thus, in C. albicans it seems that polarized growth ofhyphae is determined by two separate entities, the Spitzenkörper and the polarisome, whereasin pseudohyphae and yeast-like cells, the polarisome is responsible for polarized growth; thereis no Spitzenkörper in these cells.

F. U. maydis homologues of septinsSeptins are GTP binding proteins that are conserved from fungi to mammals and play a rolein cytokinesis and other cell processes (Gladfelter et al., 2001; Longtine and Bi, 2003; Pan etal., 2007). In S. cerevisiae, septins form filaments at the mother-bud neck region, arrangedlongitudinally (along the main cell axis) in an hour-glass shape or as horizontal rings in a cellcycle-dependent manner (Gladfeleter et al., 2001). Assembly of septins requires Cdc42,polarisome components, the PAK kinase, Cla4, and the actin cytoskeleton (Kadota et al.,2004). Septins are proposed to serve a scaffold role and recruit other proteins: bud site selectionlandmarks, components of the actomyosin contractile ring (CAR), chitin synthases, and otherproteins (Gladfelter et al., 2001; Longtine and Bi, 2003). Septins also act as diffusion barriersfor integral membrane proteins and have been proposed to serve as organizers of corticaldomains of the cell in addition to their scaffold role (Barral et al., 2000; Takizawa et al.,2000).

S. cerevisiae contains 7 septins, Cdc3, Cdc10, Cdc11, Cdc12, Sep7, Spr4, Spr28; the latter twoare meiosis-specific and required with other septins during spore maturation. The U. maydisgenome contains coding information for homologues of S. cereviase Cdc3, Cdc10, Cdc11, andCdc12 (Table 1), whereas in other filamentous fungi there appear to be at least five putativeseptins (see Borkovich et al., 2004). U. maydis Sep3, a homologue of Cdc11, is required fornormal cell morphogenesis (Boyce et al., 2005). Haploid Sep3 mutants exhibit aberrant cellmorphology: the cells are “lemon drop-shaped”, with a septum in the middle, becomemultinucleated, and have altered chitin deposition. Sep3 is also required for normalmorphology of the promycelium (a short filament produced upon germination and meiosis ofthe teliospore; Christensen, 1963), and the basidiospores (the haploid cells produced on thepromycelium by mitosis of the four primary meiotic products). Genetic analysis indicates thatSep3 acts in the cAMP signaling pathway (Boyce et et al., 2005). The role of other septins inU. maydis remains to be uncovered. In A. nidulans, AspB, a homologue of S. cerevisiae Cdc3,is hypothesized to act as a marker of branch formation. It localizes premitotically as a ring tosites of branching and secondary germ tube emergence. It also localizes postmitotically to sitesof septation (Westfall and Momany, 2002).

Banuett et al. Page 8

Fungal Genet Biol. Author manuscript; available in PMC 2009 August 1.

NIH

-PA Author Manuscript

NIH

-PA Author Manuscript

NIH

-PA Author Manuscript

G. U. maydis homologues of the exocyst complexIn S. cerevisiae, the exocyst is a protein complex required for exocytosis and consists of Sec3,Sec5, Sec6, Sec8, Sec10, Sec15, Exo70 and Exo84 (TerBush et al., 1996). It is localized to thebud tip during polarized growth and to the neck region during cytokinesis, and is involved infusion and docking of vesicles transported on actin cables. The Sec3 protein acts as a spatiallandmark for the assembly of the exocyst complex (Finger et al., 1998). The assembly of thedifferent protein complexes described above provides a temporal and spatial link between budsite selection with organization of the cytoskeleton, and secretion resulting in cell growth.

The U. maydis genome contains coding information for all the components of the exocystcomplex (Table 1) but little is known of their role in polarized growth and cytokinesis. In A.nidulans, SecC, a homologue of S. cerevisiae Sec3, accumulates at the plasma membraneanterior to the Spitzenkörper and may function as a landmark for secretion (Taheri-Talesh etal., 2008).

IV. THE CYTOSKELETONThe cytoskeleton plays an important role in cell morphogenesis and polarized growth in diverseorganisms. In U. maydis, both actin and microtubules are required for cell morphogenesis, asin other filamentous fungi.

A. The actin cytoskeletonThe actin cytoskeleton in U. maydis consists of three structures: actin patches, actin cables,and an actin ring as observed in other fungi. The actin cytoskeleton is highly polarizedthroughout the cell cycle: actin patches concentrate at the presumptive bud site and at the tipof the growing bud, and actin cables polarize towards the actin patches and extend into themother cell (Banuett and Herskowitz, 2002). During cytokinesis, actin forms a ring in the neckregion. Actin patches persist at the growing end during this process. After cell division iscomplete, both cell ends contain actin patches, with one end having a higher concentration thanthe other. This distribution of actin is consistent with highly polarized growth at the tip of thecell throughout the cell cycle. There is no evidence for a disorganized actin cytoskeleton at anystage of the cell cycle as occurs during isotropic growth in S. cerevisiae, consistent withobservations that there is no isotropic growth during bud morphogenesis in U. maydis (Banuettand Herskowitz, 2002). U. maydis hyphae contain a prominent actin cap at the tip and actincables polarize towards the tip, as observed in other filamentous fungi (Banuett andHerskowitz, 2002).

1. U. maydis homologues of components of the actin cytoskeleton—In S.cerevisiae, the actin cytoskeleton is involved in polarized secretion. Actin cables serve as trackson which vesicles move on myosin motors towards sites of active growth and secretion (thebud tip during polarized growth and the neck region during cytokinesis) (Karpova et al., 2000;Pruyne and Bretscher, 2000a,b). All components involved in actin assembly and function inS. cerevisiae appear to be conserved in the U. maydis genome (Table 1). For example, genescoding for the Arp2/3 complex (Winter et al., 1999), responsible for nucleation of branchedactin structures, are present in the U. maydis genome, as well as genes coding for homologuesof Bee1/Las17, the activator of Arp2/3 (a homologue of the mammalian Wiskott-Aldrichsyndrome protein WASP), and Vrp1 (homologue of mammalian Wip, Wiskott-Aldrichsyndrome protein interacting-protein). In S. cerevisiae, Arp2/3, Bee1/Las17, and Vrp1 localizeto actin patches and form an actin cap during early bud morphogenesis (reviewed in Pruyneand Bretscher, 2000a,b). The S. cerevisae genome contains two tropomyosin isoforms, Tpm1and Tpm2. These proteins stabilize actin cables (reviewed in Pruyne and Bretscher, 2000a,b).The U. maydis genome contains a single tropomyosin gene, and the putative protein is similar

Banuett et al. Page 9

Fungal Genet Biol. Author manuscript; available in PMC 2009 August 1.

NIH

-PA Author Manuscript

NIH

-PA Author Manuscript

NIH

-PA Author Manuscript

to S. cerevisiae Tpm2. The function of tropomyosin in U. maydis remains to be determined.The U. maydis genome contains coding information for homologues of proteins such as actinbinding protein (Abp1), coronin (Crn1), cofilin (Cof1), profilin (Pfy1), fimbrin (Sac6), Pan1,Prk1, Srv2, Sla1 and Sla2, some of which are actin patch components (Table 1). The functionof these proteins in U. maydis has not been reported. (See Moseley and Goode, 2006, for areview on the function of these proteins in S. cerevisiae).

2. U. maydis homologues of myosins—As in other filamentous fungi, the U. maydisgenome contains coding information for 4 myosins: a class I (Myo1), a class II (Myo2), a classV (Myo5), and a class XVII (myosin-chitin synthase; Csm1) (Table 1) (see Hodge and Cope,2000, for myosin classification). Myosin-chitin synthase contains an amino-terminal myosindomain and a chitin synthase domain at the carboxy terminus. It is specific to the filamentousfungi; the genomes of S. cerevisaie or S. pombe lack this information. In the yeast-like cell,Ummyo5 is required for cell morphogenesis and cell separation: Ummyo5 null mutants areviable and exhibit slow growth and formation of clusters of shorter and wider cells, which failto separate (Weber et al., 2003). Young myo5 mutant cells still exhibit polarized growth andpolarized chitin at the cell tip, whereas older cells lose polarity and become aberrantly shaped(Weber et al, 2003). In the hypha, Ummyo5 appears to be required for the axis of polarizedgrowth and to determine the area of growth: hyphae deficient in Myo5 are wider in diameterand exhibit an irregular growth pattern (spiral-like), and contain irregular deposition of chitinalong the hyphal length (Weber et al., 2003). Myo5::GFP localizes to the incipient bud site,the bud tip in cells with small buds, and becomes more dispersed in large-budded cells; inhyphae, it localizes to the tip, consistent with a role at the cell tip (Weber et al., 2003). Thefunction of Myo1 and Myo2 has not been reported. (See below for role of Csm1).

B. The microtubule cytoskeletonIn many eukaryotes, the microtubule cytoskeleton is required for polarized growth, transportof organelles and vesicles, in addition to its role in spindle assembly and function.

The microtubule cytoskeleton in U. maydis consists of an extensive cytoplasmic arraythroughout interphase that disassembles in late G2 when a short intranuclear spindle is formedand astral microtubules are assembled from the spindle pole bodies (Banuett and Herskowitz,2002; Steinberg et al., 2001; Straube et al., 2003). These astral microtubules appear to beinvolved in nuclear movements to the bud, where the nucleus divides, and then after nucleardivision, when one of the nuclei migrates to the mother cell (Banuett and Herskowitz, 2002;Fink et al., 2006; Steinberg et al., 2001). The organization of the microtubule cytoskeleton inU. maydis is more complex than that in S. cerevisiae, and is reminiscent of that observed in S.pombe. In U. maydis yeast-like cells, nucleus-associated spindle pole bodies (SPBs) nucleateastral microtubules, and cytoplasmic microtubule organizing centers (MTOCs), assembled atthe base of the bud early during bud morphogenesis, nucleate microtubules towards the budand mother cell (Straube et al., 2003). The yeast-like cell contains additional motile cytoplasmicMTOCs (Fink and Steinberg, 2006; Straube et al., 2003). In the hypha, the majority of MTsare oriented with their plus ends towards the growing tip; some MTs are oriented with theirplus ends towards the basal end of the apical cell (Schuchart et al., 2005).

The microtubule cytoskeleton is required for normal cell morphogenesis in U. maydis(Steinberg et al., 2001), just as it is in S. pombe (Sawin and Nurse, 1998; reviewed in Chang,2001). In contrast, S. cerevisiae MTs play no role in cell morphogenesis. U. maydis thusresembles S. pombe in the organization of the microtubule cytoskeleton and in the requirementof the microtubule cytoskeleton for cell morphogenesis and for determining the axis ofpolarized growth. U. maydis may thus combine strategies used by S. cerevisiae and S.pombe in novel ways to establish and maintain polarized growth and to generate cell shape.

Banuett et al. Page 10

Fungal Genet Biol. Author manuscript; available in PMC 2009 August 1.

NIH

-PA Author Manuscript

NIH

-PA Author Manuscript

NIH

-PA Author Manuscript

1. U. maydis homologues of tubulins—The U. maydis genome contains codinginformation for an α tubulin (tub1), two β tubulins, and a γ tubulin (tub2) (Table 1). Both αand γ tubulin genes have been characterized and shown to be essential for viability (Steinberget al., 2001;Straube et al., 2003). γ tubulin is found at the SPBs and also in the cytoplasmic andpolar MTOCs and its presence in these structures varies in a cell cycle dependent manner(Straube et al., 2003). α tubulin is required for cell morphology and polarized growth. One βtubulin gene was cloned, but its role in cell polarity and cell morphogenesis was not reported(Gold et al., 1994).

2. U. maydis homologues of microtubule-plus-end-associated proteins (+Tips)—+TIPs are a highly diverse group of proteins that includes MT-dependent motors andnonmotor proteins: CLIP170 (ScBik1), Dynactin (Sc Jnm1, Nip100, Arp1, Arp10), EB1 (ScBim1), CLASPS (Sc Stu1), LIS1 (Sc Pac1), Dynein (Sc Dhc1), APC (Sc Kar9), and others(Adkhmanova and Hoogenraad, 2005).

Dynein and dynactin: Cytoplasmic dynein is a multisubunit complex with a MT minus-enddirected motor activity. In U. maydis, as in other fungi, there is a single cytoplasmic dynein.The heavy chain of cytoplasmic dynein is encoded by two unlinked genes: dyn1 codes for theputative ATPase region, and dyn2 codes for the microtubule binding region (Straube et al.,2001). Dyn1 and Dyn2 polypeptides interact to form the active protein. Both genes areessential. Analysis of conditional mutations indicates that dynein is required for cellmorphogenesis, nuclear migration, microtubule organization, retrograde endosomal transport,and organization of the endoplasmic reticulum (Straube et al., 2001; Wedlich-Soldner et al.,2002). Mutant cells in either dyn1 or dyn2 lose polarity (become rounded), contain multiplenuclei that cluster in the aberrantly shaped cells and microtubules that become disorganized,and develop long projections that exhibit polarized growth (Straube et al., 2001).

Dynactin is a multiprotein complex required for activation of cytoplamic dynein-mediatedvesicular transport. It consists of at least ten polypeptides in most eukaryotes; in yeast, fourdynactin subunits have been identified (see above). The p150Glued subunit is the largest andinteracts with the 74-kDa dynein intermediate chain. Other subunits include the actin-relatedprotein Arp1/centractin (45 kDa); the 50 kDa/dynamitin subunit; dynactin p62, dynactin p27,dynactin, p25, dynactin p24/p22, and CapZ (reviewed in Schroer, 2004; Xiang and Plaman,2003). In S. cerevisiae the dynactin complex is required for nuclear migration (Lee et al.,2003; Sheeman et al., 2003). In Neurospora crassa, it is also required for nuclear migration,in addition to a role in determining the axis of polarized growth, and position of theSptizenkörper (Plaman et al., 1994; Riquelme et al., 2000; Seiler et al., 1999). The U.maydis genome contains coding information for homologues of components of the S.cerevisiae dynactin complex (Table 1), and of other dynactin components found in filamentousfungi and other eukaryotes (data not shown), and other +TIPs (Table 1). UmDya1 (thehomologue of p150 Glued), UmClip1 (CLIP170 homologue), UmLis1 (LIS1/NudFhomologue), and UmPeb1 (homologue of EB1) localize to microtubule plus ends (Lenz et al.,2006; Straube et al., 2003). UmDya1 is required for localization of dynein to microtubule plusends. UmLis1/NudF is required for activation of dynein and this activation is necessary forretrogade endosomal movement. UmClip1 is not required for retrogade endosomal movementor binding of dynein to microtubule plus ends (Lenz et al., 2006). In S. cerevisiae, Kar9 andPac1/LIS1 are required for orientation of the mitotic spoindle and nuclear migration (Lee etal., 2003; Miller and Rose, 1998; Sheeman et al., 2003). The U. maydis genome does not containcoding information for a Kar9 homologue.

3. U. maydis homologues of kinesins—In filamentous fungi, as in many othereukaryotes, kinesins are involved in long-distance transport of vesicles. S. cerevisiae contains6 kinesins whereas filamentous fungi contain 10–12 kinesins (see Borkovich et al., 2004; Xiang

Banuett et al. Page 11

Fungal Genet Biol. Author manuscript; available in PMC 2009 August 1.

NIH

-PA Author Manuscript

NIH

-PA Author Manuscript

NIH

-PA Author Manuscript

and Plamann, 2003). The U. maydis genome contains coding information for 10 kinesins (Kin1,Kin3, Kin4, Kin6, Kin7a, Kin7b, Kin8, Kin9, and Kin14), some of which are more closelyrelated to their metazoan counterparts than to the ascomycetous fungi (Schuchardt et al.,2005). Genetic analysis has shown that all except Kin1 and Kin3 are dispensable for hyphalgrowth. Null kin1 or kin3 mutants exhibit bipolar growth and short hyphae. Double kin1kin3 null mutants exhibit the same phenotype as the single mutants, indicating that they likelyact in the same pathway (Schuchardt et al., 2005). Interestingly, kin1 and kin3 mutationsexacerbate the mutant phenotype conferred by a myo5ts mutation. The residual polar growthin the myo5ts mutant is completely abolished resulting in clusters of misshapen cells that exhibitno polar growth. This synthetic interaction suggests that Kin1 and Kin3 share a common targetwith Myo5 for polarized growth. Kin1, Kin3, and Myo5 all accumulate at the hyphal apex, theregion where the Spitzenkörper localizes; however, localization of the Spitzenkörper in thesestudies was not reported.

V. U. maydis homologues of chitin synthasesIntegrity of the cell wall is crucial for maintenance of cell shape (Latge, 2007; Klis et al.,2006). Chitin and β-glucan are the major components of fungal cell walls (see article by Ruiz-Herrera in this issue). The U. maydis genome contains 7 genes that code for chitin synthases(Chs1, Chs2, Chs3, Chs4, Chs5, Chs6, Chs7) and one gene for a hybrid myosin-chitin synthaseprotein (Mcs1; see above) (Garcerá-Teruel et al., 2006; Gold and Kronstad, 1994; Weber etal., 2006). Deletion analysis of single genes indicates that Umchs1, Umchs2, Umchs3,Umchs4 are not required for morphology of the yeast-like cell or the hypha, whereas Δchs6results in cells with wider diameter, and Δmcs1 cells exhibit slightly wider cell diameter anda ballooning of the bud tip, indicative of a role in cell morphogenesis. The Umchs5 orUmchs7 null mutants exhibit a more pronounced phenotype indicative of a role in cellmorphology and cell separation, respectively: Δchs5 mutant cells are more elongated than wildtype cells, grow irregularly, and have a neck region that is not clearly defined, whereasΔchs7 mutant cells have a cell separation defect but the cells have normal cell morphology,though they are shorter, and in some cases, lose their normal cell shape (Weber et al., 2006).Six of the U. maydis chitin synthases (Chs3-Ch7 and Mcs1) localize to the septal region, andfour of them (Chs5, Chs6, Chs7, and Mcs1) also localize to the hyphal tip. Despite thelocalization of Chs5, 6, 7, and Mcs1 to the hyphal tip, they do not seem to be required forhyphal morphology in culture (Weber et al., 2006; see also Ruiz-Herrera et al., 2006). It islikely that the chitin synthases have partially overlapping functions and are able to substitutefor each other when one or two are absent. Deletion of multiple chitin synthases that localizeto the hyphal tip will likely be informative (Weber et al., 2006).

VI. FUTURE DIRECTIONSOur analysis indicates that most of the components of the S. cerevisae machinery for cellpolarity and cell morphogenesis, and the cytoskeleton are conserved in U. maydis. Becausethis analysis was based on S. cerevisiae and S. pombe genes, other components of the cellpolarity machinery specific to Ustilago maydis or the Basidiomycetes remain unidentified.Sequence comparisons with other filamentous fungi, where additional genes required forpolarized growth have been identified, in combination with genetic screens should prove usefulin obtaining a more comprehensive view of the machinery for cell polarity and cellmorphogenesis.

The challenge for the future is not only to identify the machinery for cell polarity, but also tounderstand how the components of the machinery are assembled and rearranged duringpolarized growth, and how these assemblies generate the diversity of forms that characterizethe life cycle of Ustilago maydis.

Banuett et al. Page 12

Fungal Genet Biol. Author manuscript; available in PMC 2009 August 1.

NIH

-PA Author Manuscript

NIH

-PA Author Manuscript

NIH

-PA Author Manuscript

Supplementary MaterialRefer to Web version on PubMed Central for supplementary material.

ACKNOWLDEGEMENTSWe apologize to colleagues whose work it was not possible to cite due to space limitations. We thank anonymousreviewers for their useful comments. This work was supported by NIH grants SO6 GM63119 and 2SO6 GM063119to FB, and, in part, by CONACYT grant 53191 and SNI fellowship to CRP.

LITERATURE CITEDAkhmanova A, Hoogenraad CC. Microtubule plus-end-tracking proteins: mechanisms and functions.

Curr. Opin. Cell Biol 2005;17:47–54. [PubMed: 15661518]Banuett, F. History of the mating types in Ustilago maydis. In: Heitman, J.; Kronstad, J.; Taylor, J.;

Casselton, LA., editors. Sex in Fungi: Molecular determination and evolutionary implications.Washington, DC: ASM press; 2007. p. 351-375.

Banuett, F. Pathogenic development in Ustilago maydis: A progression of morphological transitions thatresults in tumor formation and teliospore production. In: Osiewacz, HD., editor. Molecular Biologyof Fungal Development. New York, Basel: Marcel Dekker; 2002. p. 349-398.

Banuett F. Signalling in the yeasts: an informational cascade with links to the filamentous fungi.Microbiol. Molec. Biol. Rev 1998;62:249–274. [PubMed: 9618441]

Banuett F. Genetics of Ustilago maydis, a fungal pathogen that induces tumors in maize. Annu. Rev.Genetics 1995;29:179–208. [PubMed: 8825473]

Banuett F, Herskowitz I. Bud morphogenesis and the actin and microtubule cytoskeletons during buddingin the corn smut fungus, Ustilago maydis. Fungal Genet Biol 2002;37:149–170. [PubMed: 12409100]

Banuett F, Herskowitz I. Discrete developmental stages during teliospore formation in the corn smutfungus, Ustilago maydis. Development 1996;122:2965–2976. [PubMed: 8898211]

Barral Y, Mermall V, Mooseker MS, Snyder M. Compartmentalization of the cell cortex by septins isrequired for maintenance of cell polarity in yeast. Mol Cell. 2000 2000;5:841–851.

Bartnicki-Garcia, S. Hyphal tip growth: Outstanding questions. In: Osiewacz, HD., editor. MolecularBiology of Fungal Development. New York, Basel: Marcel Dekker; 2002. p. 29-58.

Bassilana M, Arkowitz RA. Rac1 and Cdc42 have different roles in Candida albicans development.Eukaryot Cell 2006;5:321–329. [PubMed: 16467473]

Bauer Y, Knechtle P, Wendland J, Helfer H, Philippsen P. A Ras-like GTPase is involved in hyphalgrowth guidance in the filamentous fungus Ashbya gossypii. Molec. Biol. Cell 2004;15:4622–4632.[PubMed: 15282338]

Borkovich KA, Alex LA, Yarden O, Freitag M, Turner GE, Read ND, Seiler S, Bell-Pedersen D, PaiettaJ, Plesofsky N, Plamann M, Goodrich-Tanrikulu M, Schulte U, Mannhaupt G, Nargang FE, RadfordA, Selitrennikoff C, Galagan JE, Dunlap JC, Loros JJ, Catcheside D, Inoue H, Aramayo R, PolymenisM, Selker EU, Sachs MS, Marzluf GA, Paulsen I, Davis R, Ebbole DJ, Zelter A, Kalkman ER,O'Rourke R, Bowring F, Yeadon J, Ishii C, Suzuki K, Sakai W, Pratt R. Lessons from the genomesequence of Neurospora crassa: tracing the path from genomic blueprint to multicellular organism.Microbiol. Molec. Biol. Rev 2004;68:1–108. [PubMed: 15007097]

Boyce KJ, Chang H, D'Souza CA, Kronstad JW. An Ustilago maydis septin is required for filamentousgrowth in culture and for full symptom development on maize. Eukaryot Cell 2005;4:2044–2056.[PubMed: 16339722]

Boyce KJ, Hynes MJ, Andrianopoulos A. Control of morphogenesis and actin localization by thePenicillium marneffei RAC homolog. J Cell Sci 2003;1:1249–1260. [PubMed: 12615967]

Boyce KJ, Hynes MJ, Andrianopoulos A. The CDC42 homolog of the dimorphic fungus Penicilliummarneffei is required for correct cell polarization during growth but not development. J Bacteriol2001;183:3447–3457. [PubMed: 11344153]

Brachmann A, Schirawski J, Müller P, Kahmann R. An unusual MAP kinase is required for efficientpenetration of the plant surface by Ustilago maydis. EMBO J 2003;22:2199–2210. [PubMed:12727886]

Banuett et al. Page 13

Fungal Genet Biol. Author manuscript; available in PMC 2009 August 1.

NIH

-PA Author Manuscript

NIH

-PA Author Manuscript

NIH

-PA Author Manuscript

Cabib E, Drgonova J, Drgon T. Role of small G proteins in yeast cell polarization and wall biosynthesis.Annu. Rev. Biochem 1998;67:307–333. [PubMed: 9759491]

Casamayor A, Snyder M. Bud-site selection and cell polarity in budding yeast. Curr. Opin. Microbiol2002;5:179–186. [PubMed: 11934615]

Chang F, Peter M. Yeasts make their mark. Nature Cell Biol 2003;5:294–299. [PubMed: 12669083]Chang F. Establishment of a cellular axis in fission yeast. Trends Genet 2001;17:273–278. [PubMed:

11335037]Chant J. Cell polarity in yeast. Annu. Rev. Cell Dev. Biol 1999;15:365–391. [PubMed: 10611966]Chen C, Ha YS, Min JY, Memmott SD, Dickman MB. Cdc42 is required for proper growth and

development in the fungal pathogen Colletotrichum trifolii. Eukaryot Cell 2006;5:155–166.[PubMed: 16400178]

Chen C, Dickman MB. Dominant active Rac and dominant negative Rac revert the dominant active Rasphenotype in Colletotrichum trifolii by distinct signaling pathways. Mol Microbiol 2004;51:1493–1507. [PubMed: 14982641]

Christensen JJ. Corn smut caused by Ustilago maydis. Am. Phytopathol. Soc. Monogr 1963;No.2:1–41.Crampin H, Finley K, Gerami-Nejad M, Court H, Galman C, Berman J, Sudbery P. Candida albicans

hyphae have a Spitzenkörper that is distinct form the polarisome found in yeast and pseudohyphae.J. Cell Sci 2005;118:2935–2947. [PubMed: 15976451]

Dong Y, Pruyne D, Bretscher A. Formin-dependent actin assembly is regulated by distinct modes of Rhosignaling in yeast. J. Cell Biol 2003;161:1081–1092. [PubMed: 12810699]

Drees BL, Sundin B, Brazeau E, Caviston JP, Chen GC, Guo W, Kozminski KG, Lau MW, Moskow JJ,Tong A, Schenkman LR, McKenzie A 3rd, Brennwald P, Longtine M, Bi E, Chan C, Novick P,Boone C, Pringle JR, Davis TN. Fields S, Drubin DG. A protein interaction map for cell polaritydevelopment. J Cell Biol 2001;154:549–571. [PubMed: 11489916]

Evangelista M, Zigmond S, Boone C. Formins: signaling effectors for assembly and polarization of actinfilaments. J. Cell Sci 2003;116:2603–2611. [PubMed: 12775772]

Finger FP, Hughes TE, Novick P. Sec3p is a spatial landmark for polarized secretion in budding yeast.Cell 1998;92:559–571. [PubMed: 9491896]

Fink G, Steinberg G. Dynein-dependent motility of microtubules and nucleation sites supportspolarization of the tubulin array in the fungus Ustilago maydis. Molec. Biol. Cell 2006;17:3242–3253. [PubMed: 16672380]

Fink G, Schuchardt I, Colombelli J, Stelzer E, Steinberg G. Dynein-mediated pulling forces drive rapidmitotic spindle elongation in Ustilago maydis. EMBO J 2006;25:4897–4908. [PubMed: 17024185]

Fischer-Parton S, Parton RM, Hickey PC, Dijksterhuis J, Atkinson A, Read ND. Confocal microscopyof FM4-64 as a tool for analysing endocytosis and vesicle trafficking in living fungal hyphae. J.Microsc 2000;198:246–259. [PubMed: 10849201]

Garcerá-Teruel A, Xoconostle-Cázares B, Rosas-Quijano R, Ortiz L, León-Ramírez C, Specht CA,Sentandreu R, Ruiz-Herrera J. Loss of virulence in Ustilago maydis by Umchs6 gene disruption. ResMicrobiol 2004;155:87–97. [PubMed: 14990260]

Gladfelter AS, Pringle JR, Lew DJ. The septin cortex at the yeast mother-bud neck. Curr Opin Microbiol2001;4:681–689. [PubMed: 11731320]

Gold SE, Kronstad JW. Disruption of two genes for chitin synthase in the phytopathogenic fungusUstilago maydis. Mol Microbiol 1994;11:897–902. [PubMed: 8022266]

Gold SE, Bakkeren G, Davies JE, Kronstad JW. Three selectable markers for transformation of Ustilagomaydis. Gene 1994;142:225–230. [PubMed: 7515016]

Guest GM, Lin X, Momany M. Aspergillus nidulans RhoA is involved in polar growth, branching, andcell wall synthesis. Fungal Genet Biol 2004;41:13–22. [PubMed: 14643255]

Harris SD, Read ND, Roberson RW, Shaw B, Seiler S, Plamann M, Momany M. Polarisome meetsSpitzenkörper: microscopy, genetics, and genomics converge. Euk. Cell 2005;4:225–229.

Harris SD. Cell polarity in filamentous fungi: shaping the mold. Intl. Rev. Cytol 2006;251:41–77.Heath, IB. Organization and function of actin in hyphal tip growth. In: Steiger, C.; Baluska, F.; Volkmann,

D.; Barlow, P., editors. Actin: a Dynamic Framework for Mulitple Plant Cell Functions. Dordrecht,Boston & London: Kluwer Academic; 2000. p. 275-300.

Banuett et al. Page 14

Fungal Genet Biol. Author manuscript; available in PMC 2009 August 1.

NIH

-PA Author Manuscript

NIH

-PA Author Manuscript

NIH

-PA Author Manuscript

Hodge T, Cope MJ. A myosin family tree. J Cell Sci 2000;113:3353–3354. [PubMed: 10984423]Holliday, R. Handbook of Genetics. In: King, RC., editor. Ustilago maydis. vol 1. New York: Plenum;

1974. p. 575-595.Jacobs CW, Mattichak SJ, Knowles JF. Budding patterns during the cell cycle of the maize smut pathogen

Ustilago maydis. Can. J. Bot 1994;72:1675–1680.Jaffe AB, Hall A. Rho GTPases: Biochemistry and Biology. Annu. Rev. Cell Dev. Biol 2005;21:347–

369. [PubMed: 16212499]Kadota J, Yamamoto T, Yoshiuchi S, Bi E, Tanaka K. Septin ring assembly requires concerted action of

polarisome components, a PAK kinase Cla4p, and the actin cytoskeleton in Saccharomycescerevisiae. Mol Biol Cell 2004;15:5329–5345. [PubMed: 15371547]

Karpova TS, McNally JG, Moltz SL, Cooper JA. Assembly and function of the actin cytoskeleton ofyeast: relationships between cables and patches. J. Cell Biol 1998;142:1501–1517. [PubMed:9744880]

Klis FM, Boorsma A, De Groot PW. Cell wall construction in Saccharomyces cerevisiae. Yeast2006;23:185–202. [PubMed: 16498706]

Klosterman SJ, Perlin MH, García-Pedrajas M, Covert SF, Gold SE. Genetics of morphogenesis andpathogenic development of Ustilago maydis. Adv. Genet 2007;57:1–47. [PubMed: 17352901]

Knechtle P, Dietrich F, Philippsen P. Maximal growth potential depends on the polarisome componentAgSpa2 in the filamentous fungus Ashbya gossypii. Molec. Biol. Cell 2003;14:4140–4154. [PubMed:12937275]

Konzack S, Rischitor PE, Enke C, Fischer R. The role of the kinesin motor KipA in microtubuleorganization and polarized growth of Aspergillus nidulans. Mol Biol Cell 2005;16:497–506.[PubMed: 15563609]

Latge JP. The cell wall: a carbohydrate armour for the fungal cell. Molec. Microbiol 2007;66:279–290.[PubMed: 17854405]

Lee W-L, OBerle JR, Cooper JA. The role of the lissencepahly protein Pac1 during nuclear migration inbudding yeast. J. Cell Biol 2003;160:355–364. [PubMed: 12566428]

Lee IH, Kumar S, Plamann M. Null mutants of the Neurospora actin-related protein 1 pointed-endcomplex show distinct phenotypes. Mol Biol Cell 2001;12:2195–2206. [PubMed: 11452013]

Leeder AC, Turner G. Characterization of Aspergillus nidulans polarisome component BemA. FungalGenet Biol. Epub. 2007

Lenz JH, Schuhardt I, Straube A, Steinberg G. A dynein loading zone for retrograde endosome motilityat microtubule plus ends. EMBO J 2006;25:2275–2286. [PubMed: 16688221]

Leveleki L, Mahlert M, Sandrock B, Bölker M. The PAK family kinase Cla4 is required for budding andmorphogenesis in Ustilago maydis. Mol Microbiol 2004;54:396–406. [PubMed: 15469512]

Longtine MS, Bi E. Regulation of septin organization and function in yeast. Trends Cell Biol2003;13:403–409. [PubMed: 12888292]

Lopez-Franco R, Bracker CE. Diversity and dynamics of the Sptizenkörper in growing hyhal tips ofhigher fungi. Protoplasma 1996;195:90–111.

Mahlert M, Leveleki L, Hlubek A, Sandrock B, Bölker M. Rac1 and Cdc42 regulate hyphal growth andcytokinesis in the dimorphic fungus Ustilago maydis. Mol Microbiol 2006;59:567–578. [PubMed:16390450]

Miller RK, Rose MD. Kar9p is a novel cortical protein required for cytoplasmic microtubule orientationin yeast. J Cell Biol 1998;140:377–930. [PubMed: 9442113]

Moseley JB, Goode BL. The yeast actin cytoskeleton: from cellular function to biochemical mechanism.Microbiol Mol Biol Rev 2006;70:605–645. [PubMed: 16959963]

Ni L, Snyder M. A genomic study of the bipolar bud site selection pattern in Saccharomycescerevisiae. Mol. Biol. Cell 2001;12:2147–2170. [PubMed: 11452010]

O'Donnell KL, McLaughlin DJ. Postmeiotic mitosis, basidiospore development, and septation in Ustilagomaydis. Mycologia 1984;76:486–502.

Pan F, Malmberg RL, Momany M. Analysis of septins across kingdoms reveals orthology and new motifs.BMC Evol Biol 2007;7:103–119. [PubMed: 17601340]

Banuett et al. Page 15

Fungal Genet Biol. Author manuscript; available in PMC 2009 August 1.

NIH

-PA Author Manuscript

NIH

-PA Author Manuscript

NIH

-PA Author Manuscript

Park HO, Bi E. Central roles of small GTPases in the development of cell polarity in yeast and beyond.Microbiol Mol Biol Rev 2007;71:48–96. [PubMed: 17347519]

Philippsen P, Kaufmann A, Schmitz H-P. Homologues of yeast polarity genes control the developmentof multinucleated hyphae in Ashbya gossypii. Curr. Opin. Microbiol 2005;8:1–8. [PubMed:15694849]

Plamann M, Minke PF, Tinsly JH, Bruno K. Cytoplasmic dynein and centractin are required for normalnuclear distribution in filamentous fungi. J. Cell Biol 1994;127:139–149. [PubMed: 7929559]

Pruyne D, Evangelista M, Yang C, Bi E, Zigmond S, Bretscher A, Boone C. Role of formins in actinassembly: nucleation and barbed-end association. Science 2002;297:612–615. [PubMed: 12052901]

Pruyne D, Bretscher A. Polarization of cell growth in yeast. I. Establishment and maintenance of polaritystates. J. Cell Sci 2000a;113:365–375. [PubMed: 10639324]

Pruyne D, Bretscher A. Polarization of cell growth in yeast. II. The role of the cortical actin cytoskeleton.2000. J. Cell Sci 2000b;113:571–585. [PubMed: 10652251]

Reynaga-Peña CG, Gierz G, Bartnicki-Garcia S. Analysis of the role of the Spitzenkörper in fungalmorphogenesis by computer simulation of apical branching in Aspergillus niger. Proc Natl Acad SciUSA 1997;94:9096–9101. [PubMed: 9256441]

Riquelme M, Bartnicki-García S, González-Prieto JM, Sánchez-León E, Verdín-Ramos JA, Beltrán-Aguilar A, Freitag M. Spitzenkörper localization and intracellular traffic of green fluoresenct protein-labeled CHS-3 and CHS_6 chitin synthases in living hyphae of Neurospora crassa. Eukaryot. Cell2007;6:1853–1864. [PubMed: 17644657]

Riquelme M, Gierz G, Bartnicki-Garcia S. Dynein and dynactin deficiencies affect the formation andfunction of the Spitzenkörper and distort hyphal morphogenesis in Neurospora crassa. Microbiol2000;146:1743–1752.

Rolke Y, Tudzynski P. The small GTPase Rac and the p21-activated kinase Cla4 in Clavicepspurpurea: interaction and impact on polarity, development and pathogenicity. Mol Microbiol2008;68:405–423. [PubMed: 18284596]

Ruiz-Herrera J, Xoconostle-Cázares B, Reynaga-Peña CG, León-Ramírez C, Cárabez-Trejo A.Immunolocalization of chitin synthases in the phytopathogenic dimorphic fungus Ustilago maydis.FEMS Yeast Res 2006;6:999–1009. [PubMed: 17042749]

Ruiz-Herrera J, León-Ramírez C, Cabrera-Ponce JL, Martínez-Espinoza AD, Herrera-Estrella L.Completion of the sexual cycle and demonstration of genetic recombination in Ustilago maydis invitro. Molec. Gen. Genet 1999;262:468–472. [PubMed: 10589834]

Rupes I, Mao WZ, Astrom H, Raudaskoski M. Effects of nocodazole and brefeldin A on microtubulecytoskeleton and membrane organization in homobasidiomycte Schizophyllum commune.Protoplasma 1995;185:212–221.

Sagot I, Klee SK, Pellman D. Yeast formins regulate cell polarity by controlling the assembly of actincables. Nature Cell Biol 2001;4:42–50. [PubMed: 11740491]

Sawin KE, Nurse P. Regulation of cell polarity by microtubules in fission yeast. J. Cell Biol1998;142:457–471. [PubMed: 9679144]

Scheffer J, Chen C, Heidrich P, Dickman MB, Tudzynski P. A CDC42 homologue in Clavicepspurpurea is involved in vegetative differentiation and is essential for pathogenicity. Eukaryot Cell2005;4:1228–1238. [PubMed: 16002649]

Scherer M, Heimel K, Starke V, Kämper J. The Clp1 protein is required for clamp formation andpathogenic development in Ustilago maydis. Plant Cell 2006 2006;18:2388–2401.

Schmitz H-P, Kaufmann A, Köhli M, Laissue PF, Philippsen P. From function to shape: a novel role ofa formin in fungal morphogenesis of the fungus Ashbya gossypii. Molec. Biol. Cell 2006;17:130–145. [PubMed: 16236798]

Schuchardt I, Assmann D, Thines E, Schuberth C, Steinberg G. Myosin-V, Kinesin-1, and Kinesin-3cooperate in hyphal growth of the fungus Ustilago maydis. Mol Biol Cell 2005;16:5191–5201.[PubMed: 16120650]

Schroer TA. Dynactin. Annu. Rev. Cell Dev. Biol 2004;20:759–779. [PubMed: 15473859]Seiler S, Plamann M. The genetic basis of cellular morphogenesis in the filamentous fungus Neurospora

crassa. Molec. Biol. Cell 2003;14:4352–4364. [PubMed: 12960438]

Banuett et al. Page 16

Fungal Genet Biol. Author manuscript; available in PMC 2009 August 1.

NIH

-PA Author Manuscript

NIH

-PA Author Manuscript

NIH

-PA Author Manuscript

Seiler S, Plamann M, Schliwa M. Kinesin and dynein mutants provide novel insights into the roles ofvesicle traffic during cell morphogenesis in Neurospora. Curr Biol 1999;9:779–785. [PubMed:10469561]

Sharpless KE, Harris SD. Functional characterization and localization of the Aspergillus nidulans forminSepA. Molec. Biol. Cell 2002;13:469–479. [PubMed: 11854405]

Sheeman B, Carvalho P, Sagot I, Geiser J, Kho D, Hoyt MA, Pellman D. Determinants of S. cerevisiaedynein localization and activation: implications for the mechanism of spindle positioning. Curr Biol2003;13:364–372. [PubMed: 12620184]

Smith DG, García-Pedrajas MD, Hong W, Yu Z, Gold SE, Perlin MH. An ste20 homologue in Ustilagomaydis plays a role in mating and pathogenicity. Eukaryot Cell 2004;3:180–189. [PubMed:14871948]

Snetselaar KM, Mim CW. Light and electron microscopy of Ustilago maydis hyphae in maize. Mycol.Res 1994;98:347–355.

Steinberg G, Wedlich-Söldner R, Brill M, Schulz I. Microtubules in the fungal pathogen Ustilagomaydis are highly dynamic and determine cell polarity. J. Cell Sci 2001;114:609–622. [PubMed:11171329]

Straube A, Brill M, Oakley BR, Horio T, Steinberg G. Microtubule organization requires cell cycle-dependent nucleation at dispersed cytoplasmic sites: polar and perinuclear microtubule organizingcenters in the plant pathogen Ustilago maydis. Molec. Biol. Cell 2003;14:642–657. [PubMed:12589060]

Straube A, Enard W, Berner A, Wedlich-Söldner R, Kahmann R, Steinberg G. A split motor domain ina cytoplasmic dynein. EMBO J 2001;20:5091–6100. [PubMed: 11566874]

Taheri-Talesh N, Horio T, Araujo-Bazán L, Dou X, Espeso EA, Peñalva MA, Osmani SA, Oakley BR.The tip growth apparatus of Aspergillus nidulans. Mol Biol Cell 2008;19:1439–1449. [PubMed:18216285]

Takeshita N, Higashitsuji Y, Konzack S, Fischer R. Apical sterol-rich membranes are essential forlocalizing cell end markers that determine growth directionality in the filamentous fungus Aspergillusnidulans. Mol Biol Cell 2008;19:339–351. [PubMed: 18003978]

Takizawa PA, DeRisi JL, Wilhelm JE, Vale RD. Plasma membrane compartmentalization in yeast bymessenger RNA transport and a septin diffusion barrier. Science 2000;290:341–344. [PubMed:11030653]

TerBush DR, Maurice T, Roth D, Novick P. The Exocyst is a multiprotein complex required forexocytosis in Saccharomyces cerevisiae. EMBO J 1996;15:6483–6494. [PubMed: 8978675]

Torralba S, Raudaskoski M, Pedregosa AM. Effects of methyl benzimidazole-2-yl carbamate onmicrotubule and actin cytoskeleton in Aspergillus nidulans. Protoplasma 1998;202:54–64.

Torralba S, Raudaskoski M, Pedregosa AM, Laborda F. Effect of cytochalasin A on apical growth, actincytoskeleton organization and enzyme secretion in Aspergillus nidulans. Microbiology 1998;144:45–53. [PubMed: 9537763]

Virag A, Lee MP, Si H, Harris SD. Regulation of hyphal morphogenesis by cdc42 and rac1 homologuesin Aspergillus nidulans. Mol Microbiol 2007;66:1579–1596. [PubMed: 18005099]

Virag A, Harris SD. Functional characterization of Aspergillus nidulans homologues of Saccharomycescerevisiae Spa2 and Bud6. Euk. Cell 2006;5:881–895.

Virag A, Griffiths AJ. A mutation in the Neurospora crassa actin gene results in multiple defects in tipgrowth and branching. Fungal Genet Biol 2004;41:213–225. [PubMed: 14732267]

Wallar BJ, Alberts AS. The formins: active scaffolds that remodel the cytoskeleton. Trends Cell Biol2003;13:435–446. [PubMed: 12888296]

Weber I, Assmann D, Thines E, Steinberg G. Polar localizing class V myosin chitin synthases are essentialduring early plant infection in the plant pathogenic fungus Ustilago maydis. Plant Cell 2006;18:225–242. [PubMed: 16314447]

Weber I, Gruber C, Steinberg G. A class V myosin required for mating, hyphal growth, and pathogenicityin the dimorphic plant pathogn Ustilago maydis. Plant Cell 2003;15:2826–2842. [PubMed:14615599]

Wedlich-Söldner R, Schulz I, Straube A, Steinberg G. Dynein supports motility of endoplasmic reticulumin the fungus Ustilago maydis. Mol Biol Cell 2002;13:965–977. [PubMed: 11907275]

Banuett et al. Page 17

Fungal Genet Biol. Author manuscript; available in PMC 2009 August 1.

NIH

-PA Author Manuscript

NIH

-PA Author Manuscript

NIH

-PA Author Manuscript

Weinzierl G, Leveleki L, Hassel A, Kost G, Wanner G, Bölker M. Regulation of cell separation in thedimorphic fungus Ustilago maydis. Molec. Microbiol 2002;45:219–231. [PubMed: 12100561]

Wendland J. Analysis of the landmark protein Bud3 of Ashbya gossypii reveals a novel role in septumconstruction. EMBO Rep 2003;4:200–204. [PubMed: 12612612]

Wendland J, Philippsen P. Cell polarity and hyphal morphogenesis are controlled by multiple rho-proteinmodules in the filamentous ascomycete Ashbya gossypii. Genetics 2001;157:601–610. [PubMed:11156982]

Westfall PJ, Momany M. Aspergillus nidulans septin AspB plays pre- and postmitotic roles in septum,branch, and conidiophore development. Mol Biol Cell 2002;13:110–118. [PubMed: 11809826]

Winter DC, Choe EY, Li R. Genetic dissection of the budding yeast Arp2/3 complex: a comparison ofthe in vivo structural roles of individual subunits. Proc. Natl. Acad. Sci 1999;96:7288–7293.[PubMed: 10377407]

Xiang X, Plamann M. Cytoskeleton and motor proteins in filamentous fungi. Curr Opin Microbiol2003;6:628–633. [PubMed: 14662360]

Yaar L, Mevarech M, Koltin Y. A Candida albicans RAS-related gene (CaRSR1) is involved in budding,cell morphogenesis and hypha development. Microbiology 1997;143:3033–3044. [PubMed:9308185]

Banuett et al. Page 18

Fungal Genet Biol. Author manuscript; available in PMC 2009 August 1.

NIH

-PA Author Manuscript

NIH

-PA Author Manuscript

NIH

-PA Author Manuscript

Figure 1. Different morphologies in the life cycle of U. maydisU. maydis exhibits two basic morphologies, a yeast-like and a filamentous form. Interactionwith the plant increases the repertoire of morphologies observed suggesting that plant signalsplay a role in reorganization of the machinery for cell polarity, cell morphogenesis, and thecytoskeleton. Panel A. Different stages of budding of haploid yeast-like cells. Panel B.Dikaryotic filaments in culture. No branching is observed. Panels C, D, E, and F. Dikaryoticfilaments growing in the plant. Panel C shows a branch (arrowhead). Panel D shows a clamp-like structure (arrowhead) (see Scherer et al., 2006). Panels E and F show multiple branches(arrowheads in Panel F). The cell wall of the plant cell is indicated an arrow. Panel G.Cylindrical cells released upon hyphal fragmentation within the tumors during teliosporeformation. Panel H. The cylindrical cells undergo morphological changes during teliosporeformation. The cells in Panels G and H are normally embedded in a mucilaginous matrix, whichmay provide osmotic support during the cell wall remodelling events occurring during thesemorphological transitions (Banuett and Herskowtiz, 1996). Inset (I). Mature teliospores withechinulate cell wall. The teliospores give rise to haploid yeast-like cells upon meiosis. Thescale bar in Panel A is 5 µm, and in Panels B, C, D, E, F, and H, 50 µm.

Banuett et al. Page 19

Fungal Genet Biol. Author manuscript; available in PMC 2009 August 1.

NIH

-PA Author Manuscript

NIH

-PA Author Manuscript

NIH

-PA Author Manuscript

NIH

-PA Author Manuscript

NIH

-PA Author Manuscript

NIH

-PA Author Manuscript

Banuett et al. Page 20Ta

ble

1U

. may

dis h

omol

ogue

s of t

he S

. cer

evisi

ae m

achi

nery

for

cell

pola

rity

, cel

l mor

phog

enes

is, a

nd th

e cy

tosk

elet

onS.

cer

evis

iae

gene

s in

volv

ed in

cel

l pol

arity

, cel

l mor

phog

enes

is, a

nd th

e cy

tosk

elet

on (c

olum

n 2)

wer

e us

ed to

pro

be th

e U

. may

dis

geno

me

with

wuB

last

at

the

MIP

S U

stila

go d

atab

ase

MU

MD

B (

http

://m

ips.g

sf.d

e/ge

nre/

proj

/ust

ilago

/), a

nd t

he U

stila

go m

aydi

sD

atab

ase a

t the

Bro

ad In

stitu

te (h

ttp://

ww

w.b

road

.mit.

edu/

anno

tatio

n/ge

nom

e/us

tilag

o_m

aydi

s/H

ome.

htm

l). W

e als

o us

ed B

last

at N

CB

I(h

ttp://

ww

w.n

cbi.n

lm.n

ih.g

ov/b

last

) (A

ltsch

ul e

t al.,

199

7). T

he g

enes

iden

tifie

d in

U. m

aydi

s wer

e th

en u

sed

to se

arch

for h

omol

ogue

sin

the

Bas

idio

myc

ota

and

Asc

omyc

ota,

and

in o

ther

euk

aryo

tes

usin

g th

e SI

MA

P to

ol a

t MIP

S (s

ee F

ig.1

S, s

uppl

emen

tary

mat

eria

l).Th

e so

urce

of

S. c

erev

isia

e ge

ne p

rodu

cts

was

Dre

es e

t al

., 20

01;

Pruy

ne a

nd B

rets

cher

, 20

00;

and

GO

ann

otat

ion

at t

heSa

ccha

rom

yces

gen

ome

data

base

(http

://w

ww

.yea

stge

nom

e.or

g/).

The

syst

emat

ic n

ame

for S

. cer

evis

iae g

enes

(col

umn

3) w

as o

btai

ned

from

(http

://w

ww

.yea

stge

nom

e.or

g/).

U. m

aydi

s gen

e nu

mbe

rs (c

olum

n 4)

wer

e ob

tain

ed fr

om (h

ttp://

mip

s.gsf

.de/

genr

e/pr

oj/u

stila

go/)

afte

r BLA

ST a

naly

sis.

E va

lues

(col

umn

5) in

dica

ted

are

as o

btai

ned

from

wuB

last

ana

lysi

s at M

IPS.

Oth

er p

aram

eter

s wer

e al

so u

sed

in o

ur B

last

ana

lysi

s, in

par

ticul

ar in

the

com

paris

on a

cros

s diff

eren

t fun

gal g

roup

s and

oth

er e

ukar

yote

s (da

ta n

ot sh

own

but a

vaila

ble

upon

requ

est).

The

last

col

umn

prov

ides

the

func

tion

of th

e S.

cer

evis

iae

gene

s (ht

tp://

ww

w.y

east

geno

me.

org/

). Th

e lis

t of g

enes

in th

isTa

ble

is n

ot c

ompr

ehen

sive

; it d

oes n

ot in

clud

e m

any

gene

s inv

olve

d in

cyt

okin

esis

, cel

l sep

arat

ion,

secr

etio

n, a

nd c

ell c

ycle

that

wer

eus

ed in

the

anal

ysis

show

n in

Fig

s 1S

(sup

plem

enta

ry m

ater

ial).

CELL

PO

LARI

TY/C

ELL

MO

RPH

OG

ENES

ISSc

gen

eSy

stem

atic

nam

eU

. may

dis M

IPS#

E v

alue

Func

tion

in S

. cer

evisi

ae1

BAG

7 Y

OR

134W

02

902

3.3e

-48

Rho

GA

P; fu

nctio

nally

rela

ted

to S

ac7

2 BE

M1

YB

R20

0W

1093

4 3.

7e-4

4 Es

tabl

ishm

ent o

f cel

l pol

arity

. Sca

ffol

d fo

r diff

eren

t pro

tein

com

plex

es

3 BE

M2

YER

155C

01

161

3.4e

-42

Rho

GA

P 4

BEM

3 Y

PL11

5C

1185

2 8.

9e-2

4 G

AP

for C

dc42

and

Rho

1 5

BEM

4 Y

PL16

1C

no

hits

In

tera

cts w

ith C

dc42

and

Rho

1. B

ud e

mer

genc

e.

6 BN

I4

YN

L233

W

no

hits

R

equi

red

for l

ocal

izat

ion

of C

HSI

II to

bud

nec

k 7

BOI1

Y

BL0

85W

03

037

1.7e

-23

Bem

1-bi

ndin

g pr

otei

n. P

olar

ized

gro

wth

8

BOI2

Y

ER11

4C

0303

7 1.

8e-1

9 B

em1-

bind

ing

prot

ein.

Pol

ariz

ed g

row

th

9 BU

D1/

RSR1

Y

GR

152C

11

909

7.8e

-49

Bud

site

sele

ctio

n. R

AS

supe

rfam

ily p

rote

in

10

BUD

2 Y

KLO

92C

01

282

6.9e

-10

Bud

site

sele

ctio

n. G

AP

for B

ud1/

Rsr

1 11

BU

D3

YC

LO14

W

no

hits

B

ud si

te se

lect

ion.

Axi

al la

ndm

ark

12

BUD

4 Y

JRO

92W

no h

its

Bud

site

sele

ctio

n. A

xial

land

mar

k 13

BU

D5

YC

RO

38C

11

476

1.3e

-12

Bud

site

sele

ctio

n. G

EF fo

r Bud

1/R

sr1

14

BUD

6/AI

P3

YLR

319C

11

657

1.6e

-70

Pola

risom

e co

mpo

nent

; int

erac

ts w

ith fo

rmin

and

act

in

15

BUD

7 Y

OR

299W

04

959

5.2e

-62

Expo

rt of

Chs

3 fr

om G

olgi

to p

lasm

a m

embr

ane.

Bip

olar

bud

ding

. 16

BU

D8

YLR

353W

no h

its

Bud

site

sele

ctio

n. B

ipol

ar la

ndm

ark

17

BUD

9 Y

GR

041W

no h

its

Bud

site

sele

ctio

n. B

ipol

ar la

ndm

ark

18

BU

D10

/AX

L2

YIL

140W

01

289

2.8e

-24

Bud

site

sele

ctio

n 19

BU

D13

Y

GL1

74W

00

191

1.1e

-10

Bud

site

sele

ctio

n. B

ipol

ar b

uddi

ng.

20

BUD

14

YA

R01

4C

0101

2 3.

4e-1

4 B

ud si

te se

lect

ion.

Bip

olar

bud

ding

. 21

BU

D15

/ED

E1

YB

L047

C

0553

3 4.

8e-6

1 B

ud si

te se

lect

ion.

Bip

olar

bud

ding

. 22

BU

D16

Y

EL02

9C

1031

0 1.

1e-4

2 B

ud si

te se

lect

ion.

Bip

olar

bud

ding

. 23

BU

D17

Y

NR

027W

10

310

1.1e

-41

Bud

site

sele

ctio

n. B

ipol

ar b

uddi

ng.

24

BUD

20

YLR

074C

04

625

2.5e

-11

Bud

site

sele

ctio

n. B

ipol

ar b

uddi

ng.

25

BUD

21

YO

R07

8W

no

hits

B

ud si

te se

lect

ion.

Bip

olar

bud

ding

. 26

BU

D22

Y

MR

014W

01

709

4.8e

-13

Bud

site

sele

ctio

n. B

ipol

ar b

uddi

ng.

27

BUD

23

YC

R04

7C

0155

1 8.

4e-6

8 B

ud si

te se

lect

ion.

Bip

olar

bud

ding

. 28

BU

D25

Y

ER01

4C-A

no h

its

Bud

site

sele

ctio

n. B

ipol

ar b

uddi

ng.

29

BUD

27

YFL

023W

no h

its

Bud

site

sele

ctio

n. B

ipol

ar b

uddi

ng.

30

BUD

31

YC

R06

3W

1005

7 1.

0e-4

6 B

ud si

te se

lect

ion.

Bip

olar

bud

ding

. 31

BU

D32

Y

GR

262C

12

089

2.3e

-20

Bud

site

sele

ctio

n. B

ipol

ar b

uddi

ng.

32

CD

C3

YLR

314C

10

503

1.1e

-117

Se

ptin

Fungal Genet Biol. Author manuscript; available in PMC 2009 August 1.

NIH

-PA Author Manuscript

NIH

-PA Author Manuscript

NIH

-PA Author Manuscript

Banuett et al. Page 21CE

LL P

OLA

RITY

/CEL

L M

ORP

HO

GEN

ESIS

Sc g

ene

Syst

emat

ic n

ame

U. m

aydi

s MIP

S#E

val

ueFu

nctio

n in

S. c

erev

isiae

33

CD

C10

Y

CR

002C

10

644

1.6e

-96

Sept

in

34

CD

C11

Y

JR07

6C

0344

9 5.

0e-7

7 Se

ptin

35

C

DC

12

YH

R10

7C

0359

9 3.

0e-9

5 Se

ptin

36

C

DC

24

YA

L041

W

0242

2 4.

2e-7

5 G

EF fo

r Cdc

42. P

olar

ity e

stab

lishm

ent

37

CD

C42

Y

LR22

9C

0029

5 1.

8e-9

0 Sm

all G

TP-b

indi

ng p

rote

in o

f RA

S su

perf

amily

. Pol

arity

est

ablis

hmen

t and

mai

nten

ance

. 38

C

HS1

Y

NL1

92W

10

117

1.5e

-169

ch

itin

synt

hase

I 39

C

HS2

Y

BR

038W

10

120

3.5e

-181

ch

itin

synt

hase

II

40

CH

S3

YB

R02

3C

1027

7.2

1.1e

-256

ch

itin

synt

hase

III

41

CH

S4/S

KT5

Y

BL0

61C

10

641

1.6e

-63

Act

ivat

or o

f chi

tin sy

ntha

se II

I 42

C

HS5

Y

LR33

0W

0284

0 7.

3e-5

3 Lo

caliz

atio

n of

chi

tin sy

ntha

se II

I 43

C

HS6

Y

JL09

9W

0495

9 1.

2e-3

2 Tr

ansp

ort o

f chi

tin sy

ntha

se II

I fro

m G

olgi

to p

lasm

a m

embr

ane

44

CH

S7

YH

R14

2W

1108

9 7.

5e-5

1 Ex

port

of C

hs3

from

ER

45

C

KA1

Y

IL03

5C

0118

0 6.

3e-1

11

Cas

ein

kina

se II

, alp

ha su

buni

t 46

C

KA2

Y

OR

061W

01

180

7.6e

-106

C

asei

n ki

nase

II, a

lpha

subu

nit

47

CK

B1

YG

L019

W

0109

4 9.

3e-5

2 C

asei

n ki

nase

II, b

eta

subu

nit

48

CK

B2

YO

R03

9W

0610

7 7.

8e-5

9 C

asei

n ki

nase

II, b

eta

subu

nit

49

CLA

4 Y

NL2

98W

10

145

1.1e

-130

PA

K fa

mily

kin

ase.

Cdc

42 e

ffec

tor

50

CLC

1 Y

GR

167W

01

316

1.4e

-17

Cla

thrin

ligh

t cha

in

51

CM

D1

YB

R10

9C

0391

0 1.

5e-4

7 C

alm

odul

in

52

CYK

3 Y

DL1

17W

no h

its

Rol

e in

cyt

okin

esis

53

D

FG5

YM

R23

8W

0607

3 1.

1e-2

2 R

equi

red

for c

ell e

long

atio

n, c

ell p

olar

ity

54

ELM

1 Y

KL0

48C

04

755

5.4e

-26

Ser/T

hr p

rote

in k

inas

e in

Sw

e1 p

athw

ay

55

END

3 Y

NL0

84C

no h

its

Endo

cyto

sis a

nd c

ytos

kele

tal o

rgan

izat

ion

56

ENT1

Y

DL1

61W

03

598

2.1e

-48

Endo

cyto

sis a

nd c

ytos

kele

tal o

rgan

izat

ion

57

ENT2

Y

LR20

6W

0359

8 1.

6e-6

6 En

docy

tosi

s and

cyt

oske

leta

l org

aniz

atio

n 58

EN

T3

YJR

125C

05

992

1.1e

-58

Rec

ruitm

ent o

f cla

thrin

59

EN

T4

YLL

038C

03

598

2.0e

-16

Endo

cyto

sis

60

FLO

8 Y

ER10

9C

0127

8 3.

1e-1

2 R

equi

red

for p

seud

ohyp

hal g

row

th

61

GIC

1 Y

HR

061C

no h

its

Cdc

42 e

ffec

tor.

Con

tain

s CR

IB d

omai

n 62

G

IC2

YD

R30

9C

no

hits

C

dc42

eff

ecto

r. C

onta

ins C

RIB

dom

ain

63

GIN

4 Y

DR

507C

03

928

1.1e

-80

Prot

ein

kina

se in

volv

ed in

bud

gro

wth

. Sim

ilar t

o K

cc4

and

Hsl

1 64

H

OF1

/CYK

2 Y

MR

032W

00

168

1.5e

-14

Req

uire

d fo

r cyt

okin

esis

. 65

H

SL1

YK

L101

W

0392

8 1.

3e-8

1 N

im-r

elat

ed p

rote

in k

inas

e; se

ptin

ring

ass

embl

y; S

we1

pat

hway

66

H

SL7

YB

R13

3C

1505

7 1.

2e-4

1 In

volv

ed in

Sw

e1 p

athw

ay

67

HYM

1 Y

KL1

89W

10

613

3.0e

-47

Cel

l mor

phog

enes

is

68

IQG

1 Y

PL24

2C

1073

0 2.

5e-4

9 C

ytok

ines

is. C

ell m

orph

olog

y.

69

KC

C4

YC

L024

W

0392

8 3.

6e-7

9 N

im-r

elat

ed k

inas

e 70

K

EL1

YH

R15

8C

1501

9 2.

0e-4

0 C

ell f

usio

n an

d ce

ll m

orph

olog

y 71

K

EL2

YG

R23

8C

1501

9 1.

9e-3

7 C

ell f

usio

n an

d ce

ll m

orph

olog

y 72

M

SB1

YO

R18

8W

no

hits

C

ell m

orph

ogen

esis

. Inv

olve

d in

regu

latio

n of

Pkc

1 an

d 1,

3-be

ta g

luca

n sy

ntha

se

73

MSB

2 Y

GR

014W

00

480

2e-4

1 M

ultic

opy

supp

ress

or o

f cdc

24 b

ud e

mer

genc

e de

fect

74

M

SB3

YN

L293

W

0093

5 3.

8e-2

2 G

TPas

e ac

tivat

ing

prot

ein

for S

ec4;

loca

lizes

to si

tes o

f pol

ariz

ed g

row

th

75

MSB

4 Y

OL1

12W

00

935

2.7e

-24

GTP

ase

activ

atin

g pr

otei

n fo

r Sec

4; lo

caliz

es to

site

s of p

olar

ized

gro

wth

76

M

UB1

Y

MR

100W

02

587

2.0e

-50

Cel

l sep

arat

ion

defe

ct; h

omol

ogue

of A

. nid

ulan

s Sam

B

77

PEA2

Y

ER14

9C

no

hits

Po

laris

ome

com

pone

nt.

78

PKC

1 Y

BL1

05C

15

023

1.4e

-230

Se

r/Thr

pro

tein

kin

ase;

cel

l wal

l int

egrit

y. L

ocal

izes

to si

tes o

f pol

ariz

ed g

row

th.

79

PLC

1 Y

PL26

8W

0298

2 2.

9e-7

5 Ph

osph

olip

ase

C. P

seud

ohyp

hal g

row

th

80

PXL1

Y

KR

090W

01

663

2.1e

-17

Mai

nten

ance

of p

olar

ized

gro

wth

. Sim

ilarit

y to

met

azoa

n pa

xilli

n 81

RA

S1

YO

R10

1W

0098

6 9.

9e-6

5 G

TPas

e in

volv

ed in

cA

MP

sign

allin

g pa

thw

ay.

82

RAS2

Y

NL0

98C

01

643

2.3e

-49

Hom

olog

ue o

f mam

mal

ian

Ras

pro

to-o

ncog

ene

83

RAX1

Y

OR

301W

00

956

6.2e

-23

Bip

olar

bud

ding

pat

tern

land

mar

k

Fungal Genet Biol. Author manuscript; available in PMC 2009 August 1.

NIH

-PA Author Manuscript

NIH

-PA Author Manuscript

NIH

-PA Author Manuscript

Banuett et al. Page 22CE

LL P

OLA

RITY

/CEL

L M

ORP

HO

GEN

ESIS

Sc g

ene

Syst

emat

ic n

ame

U. m

aydi

s MIP

S#E

val

ueFu

nctio

n in

S. c

erev

isiae

84

RAX2

Y

LR08

4C

0519

4 2.

4e-3

1 B

ipol

ar b

uddi

ng p

atte

rn la

ndm

ark

85

RDI1

Y

DL1

35C

05

693

7.8e

-33

Rho

GD

P di

ssoc

iatio

n in

hibi

tor f

or C

dc42

86

RG

A1

YO

R12

7W

0386

4 8.

3e-4

4 G

AP

for C

dc42

87

RG

A2

YD

R37

9W

0386

4 2.

0e-3

9 G

AP

for C

dc42

88

RH

O1

YPR

165W

05

734

2.7e

-78

Rho

subf

amily

. Reg

ulat

or o

f Pkc

1 an

d 1,

3-be

ta g

luca

n sy

ntha

se

89

RHO

2 Y

NL0

90W

02

494

6.4e

-54

Rho

suba

mily

pro

tein

. 90

RH

O3

YIL

118W

04

070

8.7e

-52

Rho

suba

mily

pro

tein

. 91

RH

O4

YK

R05

5W

1066

3 8.

9e-4

8 R

ho su

bam

ily p

rote

in.

92

RHO

5 Y

NL1

80C

00

295

3.5e

-52

Rho

suba

mily

pro

tein

. 93

RO

M1

YG

R07

0W

1507

0 5.

9e-1

04

GEF

for R

ho1

94

ROM

2 Y

LR37

1W

1507

0 2.

0e-1

37

GEF

for R

ho1

95

RVS1

61

YC

R00

9C

0528

3 4.

1e-6

6 A

mph

iphy

sin-

like

lipid

raft

prot

ein.

Reg

ulat

es p

olar

izat

ion

of th

e ac

tin c

ytos

kele

ton.

96

RV

S167

Y

DR

388W

01

748

1.4e

-51

Reg

ulat

ion

of a

ctin

cyt

oske

leto

n 97

SA

C7

YD

R38

9W

0290

2 1.

2e-4

3 G

AP

for R

ho1

(Fun

ctio

nally

rela

ted

to B

ag7)

98

SH

S1/S

EP7

YD

L225

W

0344

9 3.

7e-7

2 Se

ptin

99

SP

A2

YLL

021W

04

468

5.6e

-20

Pola

risom

e co

mpo

nent

10

0 SP

H1

YLR

313C

04

468

2.3e

-10

Pola

risom

e co

mpo

nent

. Hom

olog

ous t

o Sp

a2

101

SWE1

Y

JL18

7C

0633

7 5.

3e-4

0 Se

r/Thr

pro

tein

kin

ase;

invo

lved

in sw

itch

from

pol

ariz

ed to

isot

ropi

c gr

owth

10

2 W

SC1/

HC

S77

YO

R00

8C

1154

6 3.

1e-2

1 St

retc

h re

cept

or; c

ell w

all i

nteg

rity

path

way

10

3 W

SC2

YN

L283

C

no

hits

St

retc

h re

cept

or; c

ell w

all i

nteg

rity

path

way

10

4 W

SC3

YO

L105

C

1508

4 1.

6e-2

8 St

retc

h re

cept

or; c

ell w

all i

nteg

rity

path

way

10

5 W

HI3

Y

NL1

97C

04

835

2.3e

-23

Reg

ulat

or o

f cel

l siz

e. R

NA

bin

ding

pro

tein

10

6 YC

K1

YH

R13

5C

0027

4 3.

4e-1

29

Cas

ein

kina

se I

isof

orm

. Cel

l mor

phog

enes

is

107

YCK

2 Y

NL1

54C

00

274

1.6e

-126

C

asei

n ki

nase

I is

ofor

m. C

ell m

orph

ogen

esis

. Fun

ctio

nally

redu

ndan

t with

Yck

1.

108

ZDS1

Y

MR

273C

15

061.

2 4.

7e-2

0 R

egul

atio

n of

cel

l pol

arity

10

9 ZD

S2

YM

L109

W

no

hits

R

egul

atio

n of

cel

l pol

arity

. Par

alog

ue o

f ZD

S1

ACTI

N C

YTO

SKEL

ETO

NSc

gen

eSy

stem

atic

nam

eU

. may

dis M

IPS#

E v

alue

Func

tion

in S

. cer

evisi

ae11

0 AB

P1

YC

R08

8W

0534

0 7.

9e-2

3 A

ctin

-bin

ding

pro

tein

11

1 AC

F4

YJR

083C

A

ctin

cyt

oske

leto

n or

gani

zatio

n 11

2 AC

T1

YFL

039C

11

232

2.0e

-185

A

ctin

11

3 AI

P1

YM

R09

2C

0594

9 3.

0e-8

6 A

ctin

-inte

ract

ing

prot

ein;

act

in p

atch

com

pone

nt

114

APP1

Y

NL0

94W

04

613

9.7e

-22

Act

in fi

lam

ent o

rgan

izat

ion

115

ARC

15

YIL

062C

02

388

2.6e

-25

Subu

nit o

f Arp

2/3

com

plex

11

6 AR

C18

Y

LR37

0C

1024

6 7.

4e-4

4 Su

buni

t of A

rp2/

3 co

mpl

ex

117

ARC

19

YK

L013

C

1017

3 9.

8e-5

8 Su

buni

t of A

rp2/

3 co

mpl

ex

118

ARC

35

YN

R03

5C

1147

9 1.

8e-4

9 Su

buni

t of A

rp2/

3 co

mpl

ex

119

ARC

40

YB

R23

4C

0590

6 3.

7e-6

9 Su

buni

t of A

rp2/

3 co

mpl

ex

120

ARK

1 Y

NL0

20C

03

081

8.7e

-61

Act

in re

gula

ting

Ser/T

hr k

inas

e 12

1 AR

P2

YD

L029

W

0540

5 1.

7e-1

49

Subu

nit o

f Arp

2/3

com

plex

12

2 AR

P3

YJR

065C

11

265

1.2e

-139

Su

buni

t of A

rp2/

3 co

mpl

ex

123

BNI1

Y

NL2

71C

12

254

1.9e

-59

Form

in; a

ctin

nuc

leat

ion

124

BNR1

Y

IL15

9W

0114

1 2.

3e-3

1 Fo

rmin

; act

in n

ucle

atio

n. F

unct

iona

lly re

dund

ant w

ith B

ni1

125

BSP1

Y

PR17

1W

no

hits

In

volv

ed in

act

in c

ytos

kele

ton

orga

niza

tion

126

CAP

1 Y

KL0

07W

00

423

1.1e

-24

F-ac

tin c

appi

ng p

rote

in a

lpha

subu

nit

127

CAP

2 Y

IL03

4C

1117

7 2.

0e-5

0 F-

actin

cap

ping

pro

tein

bet

a su

buni

t 12

8 C

CT1

/TC

P1

YD

R21

2W

0127

9 3.

4e-2

13

Cha

pero

nin

role

for a

ctin

and

tubu

lin

129

CC

T2

YIL

142W

06

235

5.5e

-190

C

hape

roni

n ro

le fo

r act

in a

nd tu

bulin

13

0 C

CT3

Y

JL01

4W

0606

7 1.

1e-1

98

Cha

pero

nin

role

for a

ctin

and

tubu

lin

131

CC

T4

YD

L143

W

0257

1 9.

7e-1

22

Cha

pero

nin

role

for a

ctin

and

tubu

lin

132

CC

T5

YJR

064W

03

959

4.6e

-186

C

hape

roni

n ro

le fo

r act

in a

nd tu

bulin

Fungal Genet Biol. Author manuscript; available in PMC 2009 August 1.

NIH

-PA Author Manuscript

NIH

-PA Author Manuscript

NIH

-PA Author Manuscript

Banuett et al. Page 23AC

TIN

CYT

OSK

ELET

ON

Sc g

ene

Syst

emat

ic n

ame

U. m

aydi

s MIP

S#E

val

ueFu

nctio

n in

S. c

erev

isiae

133

CC

T6

YD

R18

8W

0235

0 6.

5e-1

67

Cha

pero

nin

role

for a

ctin

and

tubu

lin

134

CC

T7

YJL

111W

00

565

8.2e

-196

C

hape

roni

n ro

le fo

r act

in a

nd tu

bulin

13

5 C

CT8

Y

JL00

8C

0440

1 2.

6e-1

51

Cha

pero

nin

role

for a

ctin

and

tubu

lin

136

CH

C1

YG

L206

C

0392

1 0.

0 C

lath

rin h

eavy

cha

in

137

CO

F1

YLL

050C

04

314

3.1e

-45

Act

in b

indi

ng a

nd se

verin

g pr

otei

n 13

8 C

RN1

YLR

429W

04

417

6.5e

-107

C

ortic

al a

ctin

cyt

oske

leto

n co

mpo

nent

13

9 LA

S1

YK

R06

3C

0227

1 6.

9e-1

8 B

ud fo

rmat

ion

and

mor

phog

enes

is

140

LAS1

7/BE

E1

YO

R18

1W

0368

7 2.

8e-5

1 A

ctiv

ator

of t

he A

rp2/

3 co

mpl

ex. H

omol

ogue

of h

uman

WA

SP

141

MLC

1 Y

GL1

06W

11

848

4.0e

-29

Myo

sin

light

cha

in

142

MLC

2 Y

PR18

8C

0391

0 5.

1e-1

3 M

yosi

n lig

ht c

hain

14

3 M

YO1

YH

R02

3W

0328

6 5.

4e-1

83

Type

II m

yosi

n 14

4 M

YO2

YO

R32

6W

0455

5 2.

4e-2

76

Type

V m

yosi

n 14

5 M

YO3

YK

L129

C

1111

5 0.

0 Ty

pe I

myo

sin

146

MYO

4 Y

AL0

29C

04

555

4.5e

-258

Ty

pe V

myo

sin

147

MYO

5 Y

MR

109W

11

115

0.0

Type

I m

yosi

n 14

8 PA

N1

YIR

006C

11

804

1.3e

-40

Act

in p

atch

pro

tein

14

9 PF

Y1

YO

R12

2C

1083

2 2.

0e-2

7 Pr

ofili

n 15

0 PR

K1

YIL

095W

03

081

9.5e

-60

Ser/T

hr p

rote

in k

inas

e; re

gula

tion

of o

rgan

izat

ion

and

func

tion

of a

ctin

15

1 SA

C6

YD

R12

9C

0476

8 2.

6e-2

18

Fim

brin

; act

in fi

lam

ent b

undl

ing

prot

ein

152

SCP1

Y

OR

367W

no h

its

Com

pone

nt o

f act

in c

ortic

al c

ytos

kele

ton

153

SLA1

Y

BL0

07C

05

337

8.3e

-57

Ass

embl

y of

cor

tical

act

in c

ytos

kele

ton

154

SLA2

Y

NL2

43W

00

582

1.3e

-78

Ass

embl

y of

cor

tical

act

in c

ytos

kele

ton

155

SRV2

Y

NL1

38W

10

957

1.4e

-98

Reg

ulat

ion

of a

ctin

dyn

amic

s and

cel

l mor

phog

enes

is

156

VRP1

Y

LR33

7C

1056

6 3.

7e-4

3 V

erpr

olin

. Reg

ulat

ion

of a

ctin

cyt

oske

leto

n. H

omol

ogue

of h

uman

WIP

EX

OCY

STSc

gen

eSy

stem

atic

nam

eU

. may

dis M

IPS#

E v

alue

Func

tion

in S

. cer

evisi

ae15

7 SE

C3

YER

008C

01

107

7.2e

-27

Spat

ial l

andm

ark

for s

ecre

tion

158

SEC

5 Y

DR

166C

00

710

4.9e

-22

Subu

nit o

f the

exo

cyst

com

plex

15

9 SE

C6

YIL

068C

03

632

1.6e

-67

Subu

nit o

f the

exo

cyst

com

plex

16

0 SE

C8

YPR

055W

02

554

2.6e

-35

Subu

nit o

f the

exo

cyst

com

plex

16

1 SE

C10

Y

LR16

6C

0032

9 1.

2e-6

1 Su

buni

t of t

he e

xocy

st c

ompl

ex

162

SEC

15

YG

L233

W

0549

4 1.

1e-2

9 Su

buni

t of t

he e

xocy

st c

ompl

ex

163

EXO

70

YJL

085W

01

845

4.3e

-14

Subu

nit o

f the

exo

cyst

com

plex

16

4 EX

O84

Y

BR

102C

04

147

6.5e

-31

Subu

nit o

f the

exo

cyst

com

plex

O

THER

(SEC

RETI

ON

)Sc

gen

eSy

stem

atic

nam

eU

. may

dis M

IPS#

E v

alue

Func

tion

in S

. cer

evisi

ae16

5 SE

C4

YFL

005W

03

865

7.2e

-62

Rab

GTP

ase.

Ass

ocia

tes w

ith S

ec15

16

6 SE

C2

YN

L272

C

0055

3 7.

3e-2

3 G

EF fo

r Sec

4 M

ICRO

TUBU

LE C

YTO

SKEL

ETO

N (S

ELEC

TED

GEN

ES) D

YNEI

N/D

YNAC

TIN

(per

S. c

erev

isiae

)*Sc

gen

eSy

stem

atic

nam

eU

. may

dis M

IPS#

E v

alue

Func

tion

in S

. cer

evisi

ae16

7 D

YN1/

DH

C1

YK

R05

4C

1504

5 0.

0 H

eavy

cha

in o

f cyt

opla

smic

dyn

ein

04

372

2.6e

-150

168

DYN

2/SL

C1

YD

R42

4C

1227

8 9.

1e-2

3 D

ynei

n lig

ht c

hain

16

9 D

YN3

YM

R29

9C

0345

9&

no h

its

Dyn

ein

light

inte

rmed

iate

cha

in

170

PAC

11

YD

R48

8C

0459

8&

no h

its

Dyn

ein

inte

rmed

iate

cha

in. N

ucle

ar m

igra

tion

171

ACT5

/ARP

1 Y

HR

129C

11

692

4.2e

-105

C

ompo

nent

of t

he d

ynac

tin c

ompl

ex; r

elat

ed to

cen

tract

in

172

ARP1

0 Y

DR

106W

05

833&

no

hits

C

ompo

nent

of t

he d

ynac

tin c

ompl

ex

173

JNM

1 Y

MR

294W

02

603&

no

hits

C

ompo

nent

of t

he d

ynac

tin c

ompl

ex

174

NIP

100

YPL

174C

03

826

6.6e

-17

Com

pone

nt o

f the

dyn

actin

com

plex

. Put

ativ

e or

thol

ogue

of m

amm

alia

n p1

50G

lued

Fungal Genet Biol. Author manuscript; available in PMC 2009 August 1.

NIH

-PA Author Manuscript

NIH

-PA Author Manuscript

NIH

-PA Author Manuscript

Banuett et al. Page 24KI

NES

INS

(per

S. c

erev

isiae

)#Sc

gen

eSy

stem

atic

nam

eU

. may

dis M

IPS#

E v

alue

Func

tion

in S

. cer

evisi

ae17

5 C

IN8

YEL

O61

C

1067

8 1.

0e-9

6 K

ines

in. M

itotic

spin

dle

asse

mbl

y; c

hrom

osom

e se

greg

atio

n. R

elat

ed to

Kip

1

176

KAR

3 Y

PR14

1C

1198

6 1.

6e-8

0 K

ines

in (-

end

dire

cted

) Rel

ated

to U

m K

in14

17

7 K

IP1

YB

L063

W

1067

8 2.

5e-1

07

Kin

esin

. Fun

ctio

nally

redu

ndan

t with

Cin

8 17

8 K

IP2

YPL

155C

00

896

5.4e

-52

Kin

esin

rela

ted

mot

or p

rote

in R

elat

ed to

Um

Kin

7a a

nd K

in7b

17

9 K

IP3

YG

L216

W

0156

0 1.

7e-1

18

Kin

esin

rela

ted

mot

or p

rote

in R

elat

ed to

Um

Kin

8 18

0 SM

Y1

YK

L079

W

0421

8 3.

4e-4

5 In

tera

cts w

ith M

yo2.

N-te

rmin

al d

omai

n re

late

d to

mot

or d

omai

n of

kin

esin

s. +T

IPs

Sc g

ene

Syst

emat

ic n

ame

U. m

aydi

s MIP

S#E

val

ueFu

nctio

n in

S. c

erev

isiae

181

BIK

1 Y

CL0

29C

06

338

2.5e

-13

MT

plus

end

ass

ocia

ted

prot

ein.

Orth

olog

ue o

f mam

mal

ian

CLI

P170

18

2 BI

M1/

YEB1

Y

ER01

6W

0576

1 7.

5e-5

1 To

geth

er w

ih K

ar9

mak

es u

p th

e M

T ca

ptur

e si

te a

t the

cel

l cor

tex

183

KAR

9 Y

PL26

9W

no

hits

N

ucle

ar m

igra

tion

184

PAC

1 Y

OR

269W

03

164

7.8e

-36

LIS1

/Nud

F ho

mol

ogue

. Nuc

lear

mig

ratio

n TU

BULI

N Sc g

ene

Syst

emat

ic n

ame

U. m

aydi

s MIP

S#E

val

ueFu

nctio

n in

S. c

erev

isiae

185

TUB1

Y

ML0

85C

01

221

4.4e

-181

α–

tubu

lin

186

TUB2

Y

FL03

7W

0582

8 6.

7e-1

85

β–tu

bulin

1055

8 2.

0e-1

60

β–tu

bulin

18

7 TU

B3

YM

L124

C

0122

1 1.

5e-1

80

α–tu

bulin

18

8 TU

B4

YLR

212C

03

803

1.1e

-90

γ–tu

bulin

* C

ompo

nent

s of t

he U

. may

dis d

ynac

tin c

ompl

ex sh

own

are

per c

ompa

rison

with

S. c

erev

isia

e.

&B

last

ana

lysi

s ind

icat

es th

at th

ere

are

no h

its fo

r the

se g

enes

, how

ever

, the

U. m

aydi

s gen

e nu

mbe

rs p

rovi

ded

appe

ars t

o co

rres

pond

to th

e ye

ast g

ene.

# Kin

esin

s sho

wn

are

per c

ompa

rison

with

S. c

erev

isia

e ki

nesi

ns. S

ee a

rticl

e by

Sch

ucha

rdt e

t al.,

200

5 fo

r det

ails

of t

he k

ines

in su

perf

amily

in U

. may

dis.

Fungal Genet Biol. Author manuscript; available in PMC 2009 August 1.